Impact of Climate-induced dynamics on a Coastal
Benthic Ecosystem from the West Antarctic Peninsula
Francesca Pasotti
2015
Impact of Climate-induced dynamics on a Coastal
Benthic Ecosystem from the West Antarctic Peninsula
By
Francesca Pasotti
Promotor: Prof. Dr. Ann Vanreusel
Academic year 2014-2015
This thesis is submitted in partial fulfillment of the requirements for the degree of
Doctor in Science (Marine Sciences)
Committee members
Reading Committee
Prof. Bruno Danis (Marine Biology Laboratory, Université Libre de Bruxelles, Belgium)
Prof. Wim Vyverman (Phycology and Aquatic Ecology Laboratory, Ghent University,
Belgium)
Dr. Marleen De Troch (Marine Biology Laboratory, Ghent University, Belgium)
Examination Comittee
Dr. Elie Verleyen (Phycology and Aquatic Ecology Laboratory, Ghent University, Belgium)
Dr. Ulrike Braeckman (Marine Biology Laboratory, Ghent University, Belgium)
Prof. Dr. Tom Moens (Marine Biology Laboratory, Ghent University, Belgium)
Prof. Dr. Magda Vincx (Marine Biology Laboratory, Ghent University, Belgium)
Prof. Dr. Doris Abele (Dept. of Functional Ecology, Alfred Wegener Institute, Germany)
Prof. Wim Vyverman (Phycology and Aquatic Ecology Laboratory, Ghent University
Belgium)
Dr. Marleen De Troch (Marine Biology Laboratory, Ghent University, Belgium)
Prof. Dr. Ann Vanreusel (promoter, Marine Biology Laboratory, Ghent University,
Belgium)
Prof. Dr. Dominique Adriaens (chairman, Dept. of Evolutionary Morphology of
Vertebrates, Ghent University, Belgium)
Aknowledgments
The last lines I find myself writing are actually the first in importance for my
heart.
This PhD thesis would have never been possible without many and several
causes and conditions (hence, wonderful people) which shaped my life.
First of all, I need to thank my parents and family, who gave me this life,
nurtured me when I was little and transmitted me those basic human values
which made me go through life in a lighter, yet stronger way. Grazie mille, vi
amo.
Secondly, I want to thank my partner Inge, who has been supporting me in
this last 1.5 years of my life, a time period which has been the hardest from
all the possible points of view, yet the best ever. She never lost the patience
and gentle touch that characterise her and she gave me an amazing sense
of stability and care. Thank you, I really appreciate it.
Since we are yet at the family level, let me thank my amazing dog Blu, for all
the relaxing walks during the hard times of writing, for the tenderness in the
harsh “early wake-up” mornings, and for the loyalty that only a non-human
being can show to such a “difficult one” like me. Thank you Bluchie, I love
you.
Of course I can’t forget to thank my mentor, boss and friend Ann. Thank you
for the possibility to carry out marine biology research in one of the most
amazing ecosystems in the World, the Antarctic. Thank you for never stop
believing in me, also when I was ready to quit. Thank you for understanding
my nature, and find “alternative ways” to get the best out of me, without
braking me down. Thank you.
I wish to thank all my colleagues-friends, those in Belgium and those all
around the World (the most “famous” Marleen, Rasha, Jan, Renata,
AnnaMaria, Annelies, Isolde, Uli, Peter C., Alain, Ricardo, Leonardo, Doris,
Gaby, Lili, Dolo, Susi) for their know-how sharing, their patience, availability,
humorism and charisma. I have learnt a lot from all of you, I hope we will
keep on learning from one another.
A special thank you goes to all my friends (Simo, Michy, Tim, Gloria, Laura,
Karel, Benny, Ilias, Peter C., Peter A.) for taking care of my moods, sharing
my days and listening/sharing to my “nerd chats”. I care for each and
everyone of you, very much.
Last but not least, I want to thank all the members of the jury, for improving
and ameliorating this thesis work by the many interesting and detailed
comments I received during the review, I have found them all very
stimulating. Thank you for the work.
I wanted to keep these aknowledgments short, just because I am more a
person of facts than a person of words. I will certainly show to each and
everyone of you the appreciation, gratitude and love I feel towards you,
wonderful people of my life, who made this work possible just because life
and work are simply one thing, they support and stimulate one another
through their constant interactions.
<°(((<>< So thank you to all of you who know that I am thanking you ><>)))°>
Table of Contents
Homo immergunt
"A lot of people attack the sea, I make love to it." —
Jacques Yves Cousteau
Sea explorer
(1910 – 1997)
Table of contents
Summary.......................................................................................... i
Samenvatting ............................................................................... viii
Chapter I. General introduction
1.
Prologue: Anthropogenic climate change .............................. 1
2.
The Antarctic and climate change .......................................... 4
2.1. The ecosystem ...................................................................... 4
2.1. Recent environmental changes ............................................ 5
2.2. Biological responses to climate change in Antarctic coastal
systems ......................................................................................... 9
3.
International context ............................................................ 27
4.
Thesis background and scientific approach.......................... 29
4.1. West Antarctic coastal ecosystems: a case study............... 29
4.2. Potter Cove, King George Island, West Antarctic Peninsula30
4.3. Trophic structure at the community level: a stable isotope
approach..................................................................................... 37
4.4. Stable isotopes addition to trace carbon fluxes ................. 45
5.
Thesis outline........................................................................ 45
Chapter II. Spatial analysis
Abstract ........................................................................................ 49
1. Introduction .............................................................................. 49
2.
Material and Methods .......................................................... 51
2.1. Study sites............................................................................ 51
2.2. Environmental variables ...................................................... 52
Table of contents
2.3. Biota .................................................................................... 54
2.4. Statistical analysis ................................................................ 57
3.
Results .................................................................................. 59
3.1. Environmental variables ...................................................... 59
3.2. Biota .................................................................................... 61
4.
Discussion ............................................................................. 71
4.1. Faro ...................................................................................... 71
4.2. Isla D .................................................................................... 73
4.3. Creek.................................................................................... 75
5.
Conclusions ........................................................................... 77
6.
Acknowledgments ................................................................ 77
Chapter III. Trophic interactions
Abstract ........................................................................................ 79
1.
Introduction .......................................................................... 80
2.
Material and Methods .......................................................... 82
2.1. Study site ............................................................................. 82
2.2. Sampling and stable isotope analyses ................................. 83
2.3. Data analysis ........................................................................ 87
3.
Results .................................................................................. 90
4.
Discussion ........................................................................... 100
4.1. Temporal and spatial glacier retreat effects on benthic
trophic interactions .................................................................. 100
Table of contents
4.2. General considerations: functional traits in Potter Cove
benthic food web ..................................................................... 106
5.
Acknowledgments .............................................................. 109
Chapter IV. Temporal analysis
Abstract ...................................................................................... 113
1.
Introduction ........................................................................ 113
2.
Materials and methods ...................................................... 115
2.1. Study site and sampling strategy....................................... 115
2.2. Environmental variables .................................................... 116
2.3. Meiofaunal abundance and biomass ................................ 117
2.4. Statistical analysis .............................................................. 118
3.
Results ................................................................................ 120
3.1. Environmental description ................................................ 120
3.2. Grain size ........................................................................... 120
3.3. Sedimentary organic matter ............................................. 121
3.4. Pigments ............................................................................ 121
3.5. Meiofauna ......................................................................... 122
4.
Discussion ........................................................................... 126
4.1. Spatial differences ............................................................. 126
4.2. Seasonal differences.......................................................... 128
5.
Conclusions ......................................................................... 130
6.
Aknowledgements .............................................................. 130
Chapter V. Tracer experiment
Table of contents
Abstract ...................................................................................... 131
1.
Introduction ........................................................................ 131
2.
Materials and Methods ...................................................... 134
2.1. Sampling site and experimental design ............................ 134
2.2. Meiofauna processing and statistical analysis.................. 136
2.3. Stable isotope analysis...................................................... 136
3.
Results ................................................................................ 138
3.1. Meiobenthic community .................................................. 138
3.2. Stable isotope signatures.................................................. 143
4.
Discussion ........................................................................... 145
4.1. Meiofauna community standing stocks ........................... 145
4.2. Nematode community, diversity and structure ............... 145
4.3. Trophic ecology................................................................. 146
5.
Conclusions ......................................................................... 149
6.
Aknowledgements .............................................................. 150
Chapter VI. Sedimentation and selectivity experiments
Abstract ...................................................................................... 152
1.
Introduction ........................................................................ 153
2.
Material and Methods ........................................................ 154
2.1. Sampling site and experimental design ............................ 154
3.
Statistical analysis ............................................................... 157
4.
Results ................................................................................ 158
Table of contents
4.1. Background meiofauna assemblage ................................. 158
4.2. Sedimentation experiment (SED) ..................................... 160
4.3. Mechanical disturbance and selectivity experiment (SEL) 161
5.
Discussion ........................................................................... 163
5.1. Sedimentation experiment SED ........................................ 163
5.1. Mechanical disturbance and selectivity experiment (SEL) 169
6.
Conclusions ......................................................................... 172
7.
Aknowledgements .............................................................. 173
Chapter VII. General discussion
1.
Key findings......................................................................... 174
2. Potter Cove shallow benthos and recent rapid glacier
retreat: main insights from a two-fold investigation ................. 175
3.
General considerations and conclusions ............................ 182
4.
Methodological improvements and future directions ....... 187
Addendum
References
List of publications
A wandering iceberg
“The first time you come down for the adventure. The second for the
camaraderie. And the third time because no one else will have you.”
Anonymous
Summary
Summary
Climate change is globally recognized to pose a serious threat to
sustainable human development and to the future of our planet.
Both the palaeoclimate and the recent global warming have exhibited larger
magnitude of effects on both polar regions (the so-called polar
amplification), with some areas showing increases in mean air temperatures
double that of the global average at both poles. In the Antarctic there is a
strong regional pattern in the effects of climate change. The West Antarctic
Peninsula (WAP) region, the area hosting the highest biodiversity of the
whole Antarctic continent, is one of the fastest warming (and changing)
regions of the planet, whereas the continental Antarctic presents a general
cooling trend. In the WAP air temperatures have increased in both summer
and winter (1950-2001: summer + 2.4 ± 1.7°C century-1, autumn +6.2 ±
6.0°C century-1), the sea ice (land fastened ice – or fast ice – versus drift
and “pack” ice) ‘season’ and extent have dramatically reduced and more
than 87% of the WAP glaciers have actively retreated in the past decades.
The increases in glacier retreat observed since as early as the 1930-1950s
are coupled to intense summer glacial discharge (e.g. via glacial melt
waters), snow and permafrost melting and related effects on coastal sea
water turbidity and salinity. Moreover, the decrease in fast ice season has
led to higher frequency of iceberg scouring, the major driver of Antarctic
shelf biodiversity. All these processes affect the marine coastal
communities with direct and indirect effects. The increase in intensity of the
observed changes in the WAP appears to fall yet among the natural
variability of the past 380-2000 years of climatic history of the region, but
anthropogenic drivers are foreseen to become more important in the whole
continent by the end of 21st century. Therefore, the understanding of
biological responses to the WAP the recent environmental change context
represents a fundamental baseline for the deepening of our knowledge on
benthic assemblages ecology and their resilience to likely future changes.
In this study we investigated the benthic assemblage of Potter Cove (PC), a
fjord-like embayment located on the southern coast of King George Island
(KGI, South Shetland Islands, WAP). The cove is experiencing strong
environmental changes and rapid glacier retreat has influenced the cove
since the 1950’s. Potter Cove benthic assemblages are shaped by the
interaction of iceberg scour, which can affect the benthos down to 20 m
depth, sediment-laden melt water discharge and wave action. Recently
i
Summary
community shifts have been reported in the cove for macroepibenthic
assemblages.
With the present study we focused on the shallow soft-bottom meio- and
macrobenthos, and we deepened our investigation by looking at the
important microbiota (prokariotes and microphytobenthos) assemblage,
which is involved in the basal biogeochemical processes that model and
characterize the sediment environment in which these metazoans live. In a
spatial analysis we identified three contrasting sites (with different glacier
retreat-related history), and investigated three size classes of organisms
(microbiota, meio- and macrofauna) and interpreted their assemblage
structure in light of their different turnover rates, feeding strategies and
dispersal potential, making inferences on the historical influences of the
glacier retreat on the resident benthic communities and detecting possible
size-related biological responses. With a temporal analysis of the in situ
meiofauna standing stocks we looked at possible effects of seasonality on
the main meiofauna organisms. Moreover we contributed to the
interpretation of these results by means of laboratory experiments to unravel
potential effects of distinct glacial-related environmental stressors on PC
meiobenthos (see Fig. 1).
In the first study (Chapter II) we investigated three size classes of benthic
biota (microbenthos, meiofauna and macrofauna) at three shallow water
stations (each at a depth of 15 m) in the inner cove, which are influenced by
different glacial, meltwater, and water current conditions. Isla D (62° 13'
32.6" S, 58° 38' 32" W) is the most recently ice-free area, being exposed
since 2003, and situated about 200-215 m away from the glacier front. Faro
station (62° 13' 32.6" S, 58° 40' 03.7"W) is situated on the northern side of
the cove and became ice-free between 1988 and 1995. It is an area that is
characterized by low ice disturbance and it is affected by wave action. The
third station, “Creek” station was located adjacent to “Potter Creek” (62° 13‘
57.3" S, 58° 39’ 25.9" W). This location has been ice-free since the early
1950s and is influenced by a meltwater river that forms during summer. It is
also an area where the impact of growler ice, which can scour the benthos
in PC up to a depth of 20 m (Kowalke and Abele, 1998; Sahade et al.,
1998b). Such a study across different size spectra of the benthos is unique
for the Antarctic shallow water marine environment. Our results revealed the
presence of a patchy distribution of highly divergent benthic assemblages
within a relatively small area (about 1 km2). In areas with frequent ice
scouring and higher sediment accumulation rates, an assemblage mainly
dominated by macrobenthic scavengers (such as the polychaete Barrukia
cristata), vagile organisms, and younger individuals of sessile species
ii
Summary
(such as the bivalve Yoldia eightsi) was found. Macrofauna were low in
abundance and very patchily distributed in recently ice-free areas close to
the glacier, whereas the pioneer nematode genus Microlaimus reached a
higher relative abundance in these newly exposed sites. The most diverse
and abundant macrofaunal assemblage was found in areas most remote
from recent glacier influence. By contrast the meiofauna showed relatively
low densities in these areas. The three benthic size classes appeared to
respond in different ways to disturbances likely related to ice retreat,
suggesting that the capacity to adapt and colonize habitats is dependent
on both body size and specific life traits.
Fig. 1 Schematic view of this PhD thesis framework.
Chapter III was a continuation of the first investigation where we focused on
the trophic interactions happening at these contrasting locations. We
compared the meio- and macrofauna isotopic niche widths (δ13C and δ15N
stable isotope analysis) by means of new generation Bayesian-based
statistical approaches. The isotopic niches appeared to be locally shaped
by the different degrees of glacier retreat-related disturbance observed
within the cove. The retreat of the glacier seems to favor wider isotopic
niches lowering initial local competition. The retreat of the ice is known to
provide for new available resource pools via macroalgae colonization and
likely punctual enhanced sea ice algae sedimentation. An intermediate-high
iii
Summary
and continuous state of glacial disturbance (e.g. ice-growlers) allows new
species and new life strategies to settle during repeated colonization
processes. The smaller benthic organisms (e.g. meiofauna) seemed to be
the primary colonizers of these disturbed sediments, showing a wider
isotopic niche. Ice-scour and glacial impact hence can play a two-fold role
within the cove: i) they either stimulate trophic diversity by allowing
continuous re-colonizations of meiobenthic species or, ii) in time, they may
force the benthic assemblages into a more compacted trophic structure
with increased level of connectedness and resource recycling.
To conclude the in field work, in Chapter IV we investigated the seasonal
responses of the meiobenthic assemblage at two shallow sites, located on
the opposite shores of the inner Potter Cove (North Barton Peninsula versus
South Potter Peninsula). We focused on responses to summer/winter
biogeochemical conditions. Meiofaunal densities were found to be higher in
summer and lower in winter, although this result was not significantly related
to the in situ availability of organic matter in each season. The combination
of food quality and competition for food amongst higher trophic levels may
have played a role in determining the standing stocks at the two sites.
Meiobenthic winter abundances were sufficiently high (always above 1000
individuals per 10 cm2) to infer that energy sources were not limiting during
winter, supporting observations from other studies for both shallow water
and continental shelf Antarctic ecosystems. Recruitment within meiofaunal
communities was coupled to the local seasonal dynamics for harpacticoid
copepods but not for nematodes, suggesting that species-specific life
history or trophic features form an important element of the responses
observed.
The experimental part of the thesis starts with a tracer experiment (Chapter
V). Antarctic meiofauna trophic position in the food web is to date still poorly
studied. Primary producers, such as phytoplankton, and bacteria may
represent important food sources for shallow water metazoans and the role
of meiobenthos in the benthic-pelagic coupling represents an important
brick for food web understanding. In a laboratory feeding experiment 13Clabelled freeze-dried diatoms (Thalassiosira weissflogii) and bacteria were
added to retrieved cores from Potter Cove (15 m depth, November 2007) in
order to investigate the uptake by 3 main meiofauna taxa: nematodes,
copepods and cumaceans. In the surface sediment layers nematodes
showed no real difference in uptake of both food sources. This outcome
was supported by the natural δ13C values and the community genus
composition. In the first centimeter layer, the dominant genus was
Daptonema which is known to be opportunistic, feeding on both bacteria
iv
Summary
and diatoms. Copepods and cumaceans on the other hand appeared to
feed more on diatoms than on bacteria. This may point at a better
adaptation to input of primary production from the water column. On the
other hand, the overall carbon uptake of the given food sources was quite
low for all taxa, indicating that likely other food sources might be of
relevance for these meiobenthic organisms.
Chapter VI deals with the possible effects of climate change-related
increases in inorganic sedimentation, mechanical disturbance and changes
in food quality by means of two laboratory experiments: i) the effect of
inorganic sedimentation (SED) on the vertical distribution of the meiofauna
and ii) the effects of sediment displacement and different types of food
(SEL) on the composition of meiobenthic and nematode assemblages in
surface sediments. In the SED experiment there was no effect of the
sediment load and variances in the densities were too high to allow any
deeper understanding. In the SEL experiment the mechanical disturbance
mimicked during the collection of the natural sediment caused significant
losses in the densities of nauplii and copepods, which may have escaped
or showed to be sensitive to this type of disturbance. Among the nematode
assemblage, Aponema had an overall increase in relative abundance in the
experimental units, benefiting of the sediment mechanical re-working. The
different kind of detritus given in the microcosm (shredded macroalgae, the
benthic diatom Seminavis robusta and the haptophyte Isochrysis galbana)
did not result in significant differences among treatments in terms of
meiofaunacomposition at higher taxon level. The nematode assemblage
however, was dominated by epistrate feeders in the control and the S.
robusta treatments resembling the natural background nematode
assemblage. The macroalgae and the haptophyte detritus seemed to
stimulate the presence of non-selective deposit feeders. The genus
Sabatieria reached the highest relative abundance in these samples
compared to both the other treatment and the background sediments,
possibly because of increased hypoxic conditions in the presence of this
type of detritus. Unfortunately, the high variances found in the experimental
units hindered the finding of unequivocal effects on the nematode
assemblages in both experiments.
The data obtained in the current study indicates that Potter Cove’s shallow
benthos is responding to in situ glacial retreat with structural (biomass and
taxonomic composition) and functional (isotopic niche width) changes and
that meiofaunal organisms appear to be the most resilient size class.
Glacier retreat-related impacts on biological communities, hence, depend
on the affected organisms turnover (recruitment potential), dispersal
v
Summary
potential (capacity of re-colonisation or local migration), motility (avoidance
of ice scour impact) and dietary flexibility (resilience to overall
disturbances). The meiofauna, being connected to both the detritus and
microorganisms on the one hand and the macrofauna on the other, displays
a higher resilience to disturbance in light of an intrinsic size-dependent
centrality in the overall benthic food web and the high trophic redundancy
found between species of important taxons (e.g. nematodes). Inorganic
sedimentation per se does not affect meiofauna abundances. Nematodes
and copepods seem resilient to this disturbance. Fresh phytoplanktonic
detritus may have positive effects on their abundance. Food quality
changes (increase in macroalgae detritus and more accessible soft-celled
phytoplankton flagellates) can stimulate bacterial degradation within the
sediment and initiate short-term community shifts in the nematofauna with
genera like Sabatieria or Halalaimus becoming more abundant.
Abundances can be temporally negatively affected, especially those of
oxygen sensitive taxa (e.g. harpacticoid copepods). Ice scour seems to
have a negative effect on nematode selective feeders relative abundance.
Ice scour and wind-driven re-suspension are very important disturbances
with both “positive” and “negative” effects on the benthos, with wind
affecting depths of up to 30 m during strong storms events. Iceberg
scouring is the main driver of biodiversity in the Antarctic shelf since it
increases the spatial heterogeneity and allow more species with different
life strategies to co-exist in rather restricted areas. Anyhow, increases in
their frequency are likely to become detrimental to most macrobenthic
species, with overall strong influences, but not catastrophic consequences,
for the highly detritus based meiobenthic assemblage. Meiofauna
represents a pioneer size-class for newly ice-free, heavily scoured softbottoms, where wind-driven re-suspension is lower. Macrofauna is a poorer
competitor at high disturbances but increases its dominance at
intermediate-low disturbance levels. In the second situation competition for
resources between meiofauna and macrofauna may become more
important in shaping their relative community structure and the food web.
Future scenarios in Antarctic marine ecosystems such as PC foresee a
more or less rapid stop in iceberg scouring due to a complete withdraw of
the glacier on land and a gradual decrease in melt water discharge parallel
to KGI ice mass loss generated by the increasing temperatures. Therefore
in the future wind speed-related wave action might be the only structuring
force enacting on PC benthic communities, but to date there are no
evidences of its direct effects on these organisms. In light of the important
structuring effect of iceberg scouring and the highly hierarchical
vi
Summary
competition of Antarctic benthic assemblages, in the absence of this
forcing, we might expect, on the longer term, a general decrease in
macrobenthic resilience (both resistance to changes and recovery after
disturbance), but a rather unchanged (although fluctuating on the short
term) resilience for the meiobenthic assemblage.
vii
Summary
Samenvatting
Klimaatverandering wordt wereldwijd erkend als een ernstige bedreiging
voor de duurzame ontwikkeling en de toekomst van onze planeet.
Zowel het paleoklimaat als de recente opwarming van de Aarde hebben
een groter effect uitgeoefend op beide poolgebieden dan op de rest van de
planeet (de zogenaamde polaire amplificatie). In sommige polaire regio’s is
de toename in gemiddelde luchttemperatuur zelfs dubbel zo hoog als het
globale gemiddelde op beide polen. Op Antarctica zijn er grote regionale
verschillen
waargenomen
in
de
gevolgen
van
de
recente
klimaatverandering. Het West-Antarctische Schiereiland (WAP), het gebied
met de grootste biodiversiteit van het gehele Antarctische continent, is één
van de snelst opwarmende (en veranderende) regio's van de planeet,
terwijl het meer continentale Antarctica een algemene afkoelende trend
vertoont. In de WAP zijn de luchttemperaturen zowel in de zomer als in de
winter toegenomen (1950-2001: zomer + 2,4 ± 1,7 ° C per eeuw, herfst 6,2
± 6,0 ° C per eeuw), terwijl het zeeijsseizoen en de omvang ervan drastisch
zijn verminderd en meer dan 87% van de WAP-gletsjers sterk in omvang
zijn afgenomen de afgelopen decennia.
Het toenemende afsmelten van de gletsjers sinds de jaren 1930-1950 is
gekoppeld aan intense afvoer van terrigeen materiaal tijdens de zomer via
gletsjersmeltwater, het afsmelten van sneeuw en permafrost en andere
gerelateerde effecten die worden waargenomen in de aanpalende
kustzeeën zoals verhoogde turbiditeit en afname in saliniteit van het
zeewater. Bovendien heeft de afname van het ijsseizoen geleid tot een
hogere frequentie van ijsbergen die door het sediment ploegen, één van de
belangrijkste factoren die de biodiversiteit van het Antarctische plat
beïnvloedt. Al deze processen hebben een direct of indirect effect op het
mariene kustecosysteem. De intensiteit van de waargenomen
veranderingen in de WAP lijken echter nog te vallen binnen de natuurlijke
variabiliteit van de afgelopen 380-2000 jaar van de klimatologische
geschiedenis van de regio, maar er wordt verwacht dat antropogene
factoren belangrijker worden voor het hele continent tegen het einde van de
21e eeuw. Daarom is het cruciaal om een beter inzicht te verwerven in de
ecologische respons van de biota in de WAP regio. De recente
veranderingen in het milieu vormen een fundamentele basis voor de
verdieping van onze ecologische kennis over bodemdieren (of benthos) en
hun weerbaarheid bij veranderingen in hun milieu
viii
Summary
In deze studie werden de bodemdiergemeenschappen van Potter Cove
(PC), een fjordachtige baai gelegen aan de zuidkust van King George
Island (KGI, Zuidelijke Shetland eilanden, WAP) bestudeerd. De baai
ervaart recent sterke veranderingen in het milieu en vooral de snelle
terugtrekking van de aanpalende gletsjers heeft het aanwezige
kustecosysteem sinds de jaren 1950 sterk veranderd. De aanwezige
bodemdiergemeenschappen in Potter Cove worden immers beïnvloed door
de interactie tussen ijsbergen die tot op 20 m waterdiepte door het
sediment ploegen, maar ook door de toename in smeltwater en de
verhoogde golfslag. Verschuivingen in de macro-epibenthische component
van de bodemdiergemeenschappen in de baai werden recent reeds
gepubliceerd. Deze studie heeft zich toegespitst op de ecologie van het
meio- en macrobenthos van de zachte sedimentbodems van Potter Cove,
waarbij ook werd gekeken naar microbiotagemeenschappen (prokaryoten
en microfytobenthos), die aan de basis staan van de biogeochemische
processen die de sedimenten karakteriseren en waarin deze metazoa
leven. In de context van een ruimtelijke analyse werden drie contrasterende
locaties geïdentificeerd die een sterk verschillende voorgeschiedenis
hadden in relatie tot het afsmelten van de aanpalende gletsjers. We
onderzochten telkens drie grootteklassen binnen het benthos (microbiota,
meio- en macrofauna) waarbij de structuur van de aanwezige
gemeenschappen werd geanalyseerd aan de hand van verschillen in
taxonomische
samenstelling,
voedingsstrategieën
en
verspreidingsmechanisme. Op basis hiervan werden conclusies getrokken
over de historische impact van het afsmelten van gletsjers op de
benthische gemeenschappen en de verschillen in respons tussen de
verschillende grootteklassen. Aan de hand van een temporele analyse van
meiofaunadensiteiten en biomassa’s werd tevens gekeken naar de
eventuele seizoeneffecten. Naast deze veldwaarnemingen, werden ook
laboratoriumexperimenten uitgevoerd en hun resultaten geïntegreerd,
waarbij telkens potentiële effecten van verschillende gletsjer-gerelateerde
invloeden van het veranderende milieu op de bodemdieren, met nadruk op
het meiobenthos (zie fig. 1), werd bestudeerd.
ix
Summary
Fig. 1 Schematische voorstelling van het thesis kader.
In een eerste studie (hoofdstuk II) onderzochten we drie grootteklassen van
het benthos (microbenthos, meiofauna en macrofauna) in drie ondiepe
stations (elk op een diepte van 15 m) in het meest landinwaartse gedeelte
van de baai, dat sterk wordt beïnvloed door lokale stromingen en het
smeltwater van de verschillende gletsjers. Het station Isla D (62 ° 13 '32,6
"S, 58 ° 38' 32" W) ligt in het meest recente ijsvrij gebied, dat pas ijsvrij is
sinds 2003. Het ligt op ongeveer 200-215 meter van de gletsjer. Faro station
(62 ° 13 '32,6 "S, 58 ° 40' 03,7" W) is gelegen aan de noordelijke kant van
de baai en werd ijsvrij tussen 1988 en 1995. Het is een gebied dat wordt
gekenmerkt door een lage verstoring door ijs, maar dat wordt beïnvloed
door een sterkere golfwerking. Het derde station, "Kreek" is gelegen naast
"Potter Creek" (62 ° 13 '57,3 "S, 58 ° 39' 25.9" W). Deze locatie is ijsvrij al
sinds de vroege jaren 1950 en wordt beïnvloed door een smeltwaterrivier
die zich in de zomer vormt. Het is ook een gebied waar ijsbergen, tot op
een diepte van 20 m in het sediment schuren en zo het benthos kunnen
verstoren (Kowalke en Abele, 1998;. Sahade et al, 1998b).
Een soortgelijke studie over verschillende groottespectra van het
bodemleven is uniek voor de Antarctische kustwateren. Onze resultaten
toonden de aanwezigheid van zeer uiteenlopende benthische
x
Summary
gemeenschappen binnen een relatief klein gebied (ongeveer 1 km²). In
gebieden met frequente verstoring door ijsbergen en hogere
sedimentaccumulatie, werd een gemeenschap gevonden die gedomineerd
wordt door macrobenthische aaseters (zoals de polychaet Barrukia
cristata), mobiele organismen, en jongere individuen van sessiele soorten
(zoals de tweekleppige Yoldia eightsi). Macrofauna vertoonde lage
aantallen met een eerdere heterogene verspreiding op recent ijsvrije
plaatsten dicht bij de gletsjer, waar vermoedelijke pionierssoorten van het
nematodegenus Microlaimus ook talrijk aanwezig waren. De meest
abundante macrofaunagemeenschap werd gevonden in gebieden het verst
van de gletsjer verwijderd, en dus relatief lang ijsvrij. Uit deze ruimtelijke
analyse bleek dat drie grootteklasse van het benthos telkens anders
reageerde op de verstoringen ten gevolge van de gletsjerafbraak. Deze
resultaten suggereerden dat de manier waarop bodemorganismen zijn
aangepast aan veranderende omstandigheden verschilt naargelang
lichaamsgrootte en samenhangt met daaraan gekoppelde kenmerken.
In hoofdstuk III dat verder bouwde op de resultaten van het vorige
hoofdstuk werden de trofische interacties op deze drie contrasterende
locaties bestudeerd. We vergeleken voor meio- en macrofauna de op
isotopen gebaseerde nichebreedtes (δ13C en δ15N stabiele isotopen
analyse) door gebruik te maken van een nieuwe generatie Bayesiangebaseerde statistische benaderingen. De isotopische niches van de drie
stations verschilden naargelang de graad van gletsjer-gerelateerde
verstoring binnen de baai. Het afsmelten van de gletsjer bleek aanleiding te
geven tot bredere isotopische niches waardoor de initiële lokale
concurrentie eerder afnam. Het afsmelten van het ijs voorziet immers
nieuwe beschikbare voedselbronnen door de uitbreiding van macroalgen
maar ook ten gevolge van de verhoogde sedimentatie van ijsalgen. Een
intermediair-hoge en continue staat van verstoring ten gevolge van het
afsmelten van de gletsjer (bv door ijsbergen) laat toe dat nieuwe soorten
met andere levensstrategieën zich vestigen tijdens herhaalde
kolonisatieprocessen. De kleinere bodemdieren (bv meiofauna) blijken de
primaire kolonisatoren van deze verstoorde sedimenten te zijn, aangezien
zij een breder isotopenniche vertonen. Het afsmelten van de gletsjer kan
dus een tweevoudige rol spelen binnen de baai: i) het stimuleren van de
trofische diversiteit doordat continu rekolonisaties van meiobenthische
soorten optreden en, ii) met toenemende tijd worden de benthische
gemeenschappen in een meer compacte trofische structuur gedwongen
met een verhoogde graad van recyclage en grotere verbondenheid tussen
trofische niveaus.
xi
Summary
Tenslotte een laatste aspect van het op veldwerk gebaseerd onderzoek
komt aan bod in hoofdstuk IV waarin de seizoenale respons van de
meiobenthische gemeenschappen op twee ondiepe plaatsen, gelegen aan
tegenover elkaar liggende zijden van Potter Cove (Noord Barton
schiereiland versus Zuid Potter schiereiland) werd bestudeerd. We
concentreerden ons bij dit onderzoek op de respons van de meiofauna op
specifieke zomer/winter biogeochemische condities in het sediment.
Meiofauna densiteiten waren hoger in de zomer en lager in de winter,
hoewel dit resultaat niet significant gerelateerd was aan de in situ
beschikbaarheid van organisch materiaal. De combinatie van de
voedselkwaliteit en de concurrentie voor voedsel tussen de hogere trofische
niveaus kan een rol hebben gespeeld bij het bepalen van densiteiten op
beide tijdstippen. Meiobenthosdensiteiten waren steeds hoog tijdens de
winter (altijd boven de 1000 individuen per 10 cm2) waaruit we besloten dat
er geen tekort was aan energiebronnen in de winter, en hiermee eerdere
waarnemingen uit andere Antarctische studies zowel voor ondiep water als
het diepere continentaal plat bevestigden. Seizoensgebonden rekrutering
binnen het meiobenthos werd vooral waargenomen voor harpacticoide
roeipootkreeftjes, maar niet voor nematoden, wat suggereert dat
soortspecifieke levenscycli of trofische functies een belangrijk aspect
vormen van de waargenomen reacties.
Het experimentele deel van het proefschrift begint met een tracerexperiment (hoofdstuk V). De trofische positie in het voedselweb van
Antarctische meiofauna was immers tot dan nog niet gekend. Primaire
producenten, zoals fytoplankton, en bacteriën kunnen een belangrijke
voedselbron vormen voor ondiep water metazoa en de rol van meiobenthos
in de benthische-pelagische koppeling vormt een belangrijke schakel voor
een beter begrip van het aanwezige voedselweb. In een ex situ
voedingsexperiment werden met 13C-gemerkte en gevriesdroogde
diatomeeën (Thalassiosira weissflogii) en bacteriën toegevoegd aan
onverstoorde bodemstalen van Potter Cove (15 m diepte, november 2007).
Op deze manier kon de voedselopname door 3 belangrijke meiofauna taxa,
nematoden, roeipootkreeftjes en cumaceans, worden onderzocht. In de
oppervlakkige sedimentlagen toonden de nematoden geen significant
verschil in opname van beide voedselbronnen. Deze resultaten werd verder
aangevuld
met
de
natuurlijke
δ13C
waarden
en
de
gemeenschapssamenstelling van de nematoden. In de bovenste laag van
het sediment behoorde de dominante soort tot het genus Daptonema,
waarvan vele soorten gekend zijn als opportunisten die zich met zowel
bacteriën als diatomeeën voeden. Copepoden en cumaceeën blijken zich
meer te voeden met diatomeeën dan met bacteriën. Dit kan wijzen op een
xii
Summary
betere aanpassing aan de toevoer van primaire productie uit de
waterkolom. Anderzijds was de totale opname van koolstof van beide
voedselbronnen eerder laag voor alle taxa, wat aangeeft dat waarschijnlijk
ook andere voedingsbronnen van belang kunnen zijn voor deze
meiobenthische organismen.
Hoofdstuk VI wil het effect nagaan van verschillende verstoringen die het
gevolg kunnen zijn van het afsmelten van gletsjers waaronder de toename
in anorganische sedimentatie, mechanische storing door ijsbergen en
veranderingen in de kwaliteit van het voedsel. Dit gebeurde op basis van
twee labo-experimenten waarbij het volgende werd getest: i) het effect van
anorganische sedimentatie (SED) op de verticale verdeling van de
meiofauna en ii ) de gevolgen van sedimentverplaatsing en verschillende
soorten voedsel (SEL) op de samenstelling van het meiobenthos en meer
specifiek de nematodengemeenschappen in de oppervlakkige sedimenten.
In het SED experiment was er geen duidelijk effect van de hoeveelheid
sediment gezien de hoge variaties in densiteiten waargenomen binnen een
zelfde behandeling. In het SEL experiment werd de mechanische verstoring
van ijsbergen nagebootst, door verstoord oppervlaktesediment uit de baai
in het labo te plaatsten en op te volgen. Nauplii larven en roeipootkreeftjes,
bleken erg gevoelig voor dit type verstoring. Bij de nematoden vertoonde
het genus Aponema een duidelijke toename in aantallen. De verschillende
soorten detritus die in deze microcosm studie werden toegevoegd,
waaronder versnipperde macroalgen, de benthische diatomeeën Seminavis
robusta en de Haptophyta Isochrysis Galbana) leidden niet tot significante
verschillen tussen de behandelingen in termen van meiofaunacompositie
op hoger taxon niveau. De nematodegemeenschappen werden echter
gedomineerd door ‘epistratum feeders’ (2A) in de controlegroep, terwijl de
S. robusta behandelingen het meest gelijkenis vertoonden met de
gemeenschappen in de natuurlijke sedimenten. De macroalgen en
Haptophyta detritus leek de aanwezigheid van niet-selectieve ‘deposit
feeders’ (1B) te stimuleren. Het genus Sabatieria bereikte de hoogste
relatieve abundantie in deze behandelingen, mogelijk vanwege hypoxische
omstandigheden in aanwezigheid van dit soort detritus. Helaas, de hoge
varianties die werden gevonden in de experimentele eenheden bemoeilijkte
opnieuw
het
vinden
van
eenduidige
effecten
op
de
nematodegemeenschappen in beide experimenten.
De gegevens die zijn verkregen in deze studie zijn grotendeels in
overeenstemming met resultaten uit reeds aanwezige literatuur, en toonden
aan dat het benthos van het ondiepe gedeelte van Potter Cove
xiii
Summary
uitgesproken reageert op in situ veranderingen ten gevolge van de zich
terugtrekkende gletsjer, met zowel structurele (biomassa en taxonomische
samenstelling) als functionele (isotopen niche breedte) veranderingen als
gevolg. Verder blijken de meiobenthische organismen het meest bestand
tegen deze veranderingen. Gletsjer-gerelateerde effecten op biologische
gemeenschappen, zijn dus, afhankelijk van de taxa-specifieke turnover
(rekruteringspotentieel), hun potentiële verspreidingsgebied (capaciteit van
re-kolonisatie of lokale migratie), hun mobiliteit (het vermijden van impact
door ijsbergen) en hun trofische flexibiliteit (algemene veerkracht). De
meiofauna, enerzijds afhankelijk van detritus en micro-organismen, maar
anderzijds ook verbonden met de macrofauna, is beter bestand tegen
verstoring gekoppeld aan hun intrinsieke grootte-afhankelijke centrale rol in
het benthische voedselweb en de hoge trofische redundantie gevonden
tussen belangrijke taxa (bv nematoden). Anorganische sedimentatie op
zich heeft geen invloed op totale meiofauna abundanties, en zowel
nematoden als roeipootkreeftjes lijken bestand tegen deze verstoring. Vers
fytoplanktondetritus kan een positief effect hebben op hun aantallen.
Veranderingen in voedselkwaliteit (toename van macroalgendetritus en
ééncellige fytoplanktonische flagellaten) kan bacteriële degradatie binnen
het sediment stimuleren en op korte termijn verschuivingen veroorzaken in
de nematodengemeenschappen met toename in genera zoals Sabatieria of
Halalaimus. Abundanties van zuurstofgevoelige taxa (bv harpacticoide
copepoden) kunnen ook tijdelijk negatief worden beïnvloed. Mechanische
verstoring lijkt een negatief effect te hebben op de nematode selectieve
feeders (1A).
Verstoring van het sediment door ijsbergen en resuspensie van sedimenten
zijn erg belangrijk verstoringen met zowel 'positieve' en 'negatieve' effecten
op het bodemleven. Verstoring door ijsbergen is één van de belangrijkste
factoren verantwoordelijk voor de hoge biodiversiteit in de Antarctische
shelf, omdat de ruimtelijke heterogeniteit wordt verhoogd en daardoor meer
soorten met verschillende levensstrategieën naast elkaar kunnen bestaan in
beperkte gebieden. Echter verhoogde frequenties van deze verstoringen
zijn waarschijnlijk schadelijk voor de meeste macrobenthossoorten, en
hebben tevens een strek impact, zij het niet catastrofaal, op de eerder
detritusafhankelijke
meiofaunagemeenschappen.
Meiofauna
vertegenwoordigt een pioniersfunctie voor nieuw ijsvrije zachte bodems,
waar resuspensie onder invloed van golfwerking eerder laag is. Macrofauna
is een zwakkere concurrent bij hoge verstoringen maar verhoogt zijn
dominantie op intermediaire lagere verstoringsniveaus. In dit laatste geval
kan er concurrentie optreden tussen meiofauna en macrofauna, met
gevolgen voor de relatieve gemeenschapsstructuur en het voedselweb.
xiv
Summary
Toekomstscenario's in Antarctische mariene ecosystemen zoals PC
voorspellen een min of meer snelle afname in de mechanische verstoring
van het sediment door ijsbergen doordat de gletsjer zich volledig zal
terugtrekken op land. Ook zal er een geleidelijke afname zijn van het
smeltwater in parallel met KGI ijsmassaverlies gegenereerd door de
stijgende temperaturen. Daarom zal in de toekomst de aan hoge
windsnelheid gerelateerde golfslag misschien de enige structurerende
factor zijn voor de benthische gemeenschappen in Potter Cove, maar tot op
heden zijn er geen bewijzen van directe effecten van deze factor op de
aanwezige organismen. In het licht van de belangrijke structurerende
werking van ijsbergverstoring en de sterk hiërarchische structuur van
Antarctische gemeenschappen in de afwezigheid van deze verstoring,
voorspellen we op de langere termijn een algemene daling van de
macrobenthische veerkracht (zowel weerstand tegen veranderingen en
herstel na verstoring), maar een vrij onveranderde (hoewel fluctuerende op
de korte termijn) veerkracht voor de meiobenthische gemeenschappen.
xv
Chapter I. General introduction
Carlini Base, King George Island, West Antarctic Peninsula
“I have come to the conclusion that life in the Antarctic Regions can be very
pleasant”
Robert F. Scott
Antarctic explorer
(1868-1912)
Chapter I. General introduction
1.
Prologue: Anthropogenic climate change
The Earth is an open system that receives heat from the Sun and radiates it
back into space. To keep a constant temperature, the Earth must radiate as
much energy as it receives. Without the presence of an atmosphere and the
gases that form this atmosphere, the Earth would be close to freezing point
given its distance from the Sun. The greenhouse effect is therefore the
process whereby the thermal radiation that is emitted by the land and
ocean is reabsorbed by the atmosphere and reradiated back to the planet’s
surface. Earth’s climate history has fluctuated between a “greenhouse
Earth” (or “hotearth”, with higher greenhouse gas concentrations and higher
temperatures) and an “icehouse Earth” (experiencing an ice age, with lower
greenhouse gases concentrations, cooler temperatures and the presence
of continental ice sheets), each lasting millions of years (Price et al., 1998).
During an ice age the Earth’s ice sheets wax and wane through several
glacial (colder) and interglacial (warmer) periods within each glacial cycle
(Petit et al., 1999). All these processes are tuned and tightly linked to the
Earth’s water and carbon cycles (amongst others) and to plate tectonic
dynamics. Only a fraction of one percent of our modern atmosphere is
composed by carbon dioxide (CO2), methane (CH4) and nitrous oxide (N2O)
(among others), gases which can trap heat and therefore contribute to the
greenhouse effect. However, the concentrations of these gases have varied
widely during Earth’s history in parallel with cycles of the many
glacial/interglacial periods (Petit et al., 1999). Prior to the “Great Oxidation
Event” (c.a. 2.4 Ga ago) (Buick, 2008) the Earth’s atmosphere was mostly
composed of CO2, but the evolution of photosynthetic life on Earth is among
the causes of the gas’ subsequent drop in concentration. The sequestration
of atmospheric carbon into photosynthetic organism biomass led to the
decline in atmospheric CO2 concentration and may have contributed to the
formation of the so-called “snowball Earth” around 2.3 Ga (Buick, 2008;
Coetzee et al., 2006; Kasting et al., 1987), although the existence of such a
hard snow-shelled planet has been recently challenged by boron and triple
oxygen stable isotopes analysis of Brasilian cap carbonates (Sansjofre et
al., 2011).
The Earth is currently in an interglacial period which commenced as ice
sheets retreated after the Last Glacial Maximum around 20,000 years ago,
the Holocene (from Greek ὅλος (holos, whole or entire) and καινός (kainos,
new). This period has seen relative climatic stability and it encompasses the
development and flourishing of human society and the worldwide impacts
that the human species have brought upon global natural cycles. In a
nutshell, humans have enormously modified the environment they live in
1
Chapter I. General introduction
since the so-called Neolithic Demographic Transition (or I st agricultural
revolution, 14,000-5,000 years B.P.), a period during which human cultures
abandoned hunter-gatherer nomadism, rather embracing an agriculturebased life-style that led to conspicuous human population growth in
permanent settlements (villages, towns and cities) supported by growing
production of crops and livestock. In the more recent past, during the
Industrial Revolution (1760-1840 C.E.), a sharp shift from wood to fossil
fuels (coal, oil and gas) as the main source of energy catalysed industrial
mass production (of goods, crops and livestock) and the worldwide fuelbased transport network system, unbalancing all Earth’s natural cycles.
Extended deforestation, high rates of species extinction, a steep increase in
greenhouse gas emissions and consequent global mean air temperature
rise are among the major impacts of industrial and post-industrial human
society. Worth noting, the impact of the human species on the Earth’s
ecosystems is regarded by some authors to be great enough to justify the
erection of a new geological epoch – the Anthropocene (Braje and
Erlandson, 2013; Smith and Zeder, 2013).
In 1988 the Intergovernmental Panel on Climate Change (IPCC) was
established by the United Nations Environment Programme (UNEP) and the
World Meteorological Organisation (WMO) “to provide the world with a clear
scientific view on the current state of knowledge on climate change and its
potential environmental and socio-economic impacts”. Among the scientific
community, a consensus on the anthropogenic nature of current global
warming has only recently (1996-2009) been achieved (Cook et al., 2013).
In 2013 the IPCC stated “Warming of the climate system is unequivocal, as
is now evident from observations of increases in global average air and
ocean temperatures, widespread melting of snow and ice, and rising global
mean sea level”. Today, climate change is globally recognized to pose a
serious threat to sustainable human development and to the future of our
planet.
Since the pre-industrial period, atmospheric CO2 concentration has risen
from 280 ppm to 379 ppm in 2005. Recently at Mauna Loa (Hawaii) the CO 2
concentrations spiked several times above 400 ppm, a value “not reached
at this key surveillance point for a few million years” (Monastersky, 2013). In
2005, studies carried out on the Antarctic Vostok and EPICA Dome C ice
cores showed how this concentration exceeded anything in the natural
range over the past 650 000 – 800 000 years (see Fig. 1, IPCC, 2013; Lüthi
et al., 2008; Siegenthaler et al., 2005). By analysing δD (proxy for air
temperatures) as a function of CO2, these studies found a significantly
stable coupling between climate temperatures and the carbon cycle during
the late Pleistocene (see Fig. 1 from Lüthi et al., 2008). Based on several
2
Chapter I. General introduction
Fig. 1 CO2 records and EPICA Dome C temperature anomalies for the past 800 000
years. The Dome C temperature anomaly (black step curve) record was estimated
with respect to the mean temperature of the last millennium based on original δD data
interpolated to a 500-yr resolution. CO2 data are from Dome C (solid circles in purple,
blue, black and red), Taylor Dome (brown) and Vostok (green). From Lüthi et al.
(2008).
independently produced datasets, global averaged land and ocean surface
temperatures show a linear warming of 0.85°C (0.65°C lower mean
warming; 1.06°C higher mean warming), over the period 1880 – 2012
(IPCC, 2013). On average the global amounts of snow and ice have
diminished, glaciers have continued to shrink and mean sea level has risen
by 0.19 m (0.17 m lower mean sea level rise; 0.21 m higher mean sea level
rise) in the period 1901 - 2010 (IPCC, 2013).
The vast volume and inertia of the oceans play an important role as buffer
for these changes. First, through sequestrating heat from the warming
atmosphere and releasing water vapour they have cooling effects on the
stratosphere (Garfinkel et al., 2013; Qian et al., 2013; Qiang, 2013) and,
second, by serving as a carbon sink absorbing atmospheric CO 2 through
diffusion (although this also leads to ocean acidification, IPCC, 2007) and
the biological carbon pump (Sarmiento et al., 1998), they reduce the rate of
increase of CO2 concentration in the atmosphere. The acidification of the
Earth’s water masses has been linked to pre-historical mass extinctions
(Beerling, 2002; Veron, 2008), and recent studies warn of the possible
3
Chapter I. General introduction
extinction of important calcifying organisms within the current century
(Cummings et al., 2011; Ellis et al., 2009; Guy et al., 2014; O’Donnell et al.,
2009; Orr et al., 2005). However, feedbacks of the ocean carbon cycle on
climate change are yet to be completely understood (Cox et al., 2000). All
these global environmental changes together with other anthropogenic
stressors (e.g. land use change, habitat destruction, overfishing, pollution)
are posing a serious threat to the world’s natural systems (Convey, 2011;
Hansell et al., 1998; Malcolm et al., 2006; Parmesan and Yohe, 2003).
2.
The Antarctic and climate change
2.1. The ecosystem
Antarctica is the southernmost continent on Earth, surrounded by about
34.8 million km2 of ocean, the Southern Ocean (SO) (Fig. 2). On average, it
is the coldest (Vostok station extreme minimum recorded on Earth: -89°C),
driest continent (rainfall equivalent 166 mm year -1), it has experienced the
strongest winds ever recorded (Base Belgrano II: 351 km/h), and has sea
water which can reach the coldest temperatures (down to -1.9°C). In light of
its polar position (the Antarctic Circle lies at 66°33' S) the Antarctic is
strongly seasonal in terms of light/darkness periods and hence of primary
production, the latter also being influenced by the annual advance and
retreat of the sea-ice (Smith et al., 2001), which effectively doubles the area
of the continent in winter. Antarctica is a very complex, interconnected
system where interactions between the atmosphere, ocean, ice and biota
are non-linear (Convey et al., 2009a; Turner et al., 2009, 2013) and in which
variability operates on time scales from million/thousands of years through
decadal and seasonal to instantaneous.
The separation of the Antarctic continent from Australia across the Tasman
Rise and the formation of the Drake passage south of South America (~32
Mya and 30-24 Mya respectively, Hassold et al., 2009; Lawver & Gahagan,
2003 and references therein), permitted the development of the fastest and
largest (in terms of water mass transport) current in the world, the Antarctic
Circumpolar Current (ACC), encircling the continent from the surface to
about 3000-3500 m depth (Barnes et al., 2006), and driven by strong
westerly winds. The development of this oceanic barrier effectively isolated
the Southern Ocean and Antarctic continent from lower latitudes,
accelerating processes of continental and regional cooling that were
already occurring. This catalysed the development of the cold temperature
regimes characteristic of the Antarctic land and ocean, eventually
4
Chapter I. General introduction
permitting the formation of permanent continental-scale ice sheets. Shelf
and shallow water marine ecosystems (up to > 1000 m depth) in the
Antarctic are isolated from the other oceans by one of the eastward flowing
jets of the ACC, the Polar Front (PF) (Barnes et al., 2006). This
biogeographic discontinuity is generated by a steep temperature gradient
of 3-4°C on a distance of tens of kilometers (Convey et al., 2014 and
references therein) and it is reflected by the low number of epipelagic or
benthic taxa with a distribution both inside and outside the SO (Dell, 1972).
Nevertheless, the SO plays a vital role in the global ocean circulation
system (the ‘ocean conveyor belt’), as it is connected to and feeds the
Pacific, Atlantic and Indian Oceans with the formation of deeper waters of
variable characteristics (Mantyla and Reid, 1983). The combination of a
long history of isolation, the geological- and seasonal-scale of sea ice
dynamics, the low but stable temperature conditions of the SO water
masses and the marked seasonality in primary production had and still
have enormous consequences for the speciation, evolution and vulnerability
of the highly diverse Antarctic marine life (Aronson et al., 2007; Brandt,
2005; Clarke, 1988; Clarke et al., 2004; Clarke & Crame, 2010; Convey et
al., 2014; Griffiths, 2010).
2.1. Recent environmental changes
Despite its oceanic isolation, the Antarctic climate system is tightly
interlinked to the rest of the Earth’s system mainly via the atmosphere’s
circulation and associated teleconnections. Observed climatic changes in
the Antarctic continent are spatially variable (Fig. 3). Since the 1950s
atmospheric temperatures have increased (Faraday/Vernadsky station
record 1950-2001: summer +2.4± 1.7°C century-1, fall +6.2 ± 6.0°C century1
) in the Antarctic Peninsula (AP), with the West Antarctic Peninsula (WAP)
being among the fastest warming regions on Earth (Turner et al., 2009,
2013; Vaughan et al., 2003). These increases have been related to the
influence of the main climatic variabilities that act on the AP region: the El
Niño Southern Oscillation (ENSO) – and related La Niña - and the Southern
ocean Annular Mode (SAM). The warming of the summer season has been
related to a positive phase in the SAM (Thompson & Solomon, 2002;
Marshall, 2007) which is also likely responsible for the increase in the
westerly circumpolar winds (possibly a consequence of the anthropogenic
ozone hole, Cai, 2006; Polvani et al., 2011). On the other hand, the austral
autumn and spring surface temperature increases have been linked to
forcing resulting from the sea surface temperature anomalies of the tropical
Pacific (Ding and Steig, 2013; Turner, 2004).
5
Chapter I. General introduction
Fig. 2 Map of the Antarctic and the Southern Ocean (Convey et al., 2014, courtesy of
Peter Convey, BAS).
Relationships between the ENSO and the AP have been mostly persistent in
its Western part, whereas the SAM seemed to have major influence on the
air temperature changes of the North Eastern part, although these
relationships are yet to be totally understood (Clem and Fogt, 2013).
Usually, El Niño (warming) events in the Pacific bring cooling in the WAP,
with increases in sea ice extent and duration (Stammerjohn et al., 2008), but
not all El Niño events produce similar responses over the Bellingshausen
Sea (Meredith et al., 2008; Turner, 2004). A positive phase of the SAM
instead, increases the westerly winds leading to the upwelling of warmer
Circumpolar Deep Waters (CDW) along the coastlines of the Amundsen and
Bellingshausen seas (Jacobs et al., 2011; Jacobs & Comiso, 1997; Holland
et al., 2010). This process is thought to underlie ice shelf thinning and
collapse in this region due to basal melting (Oppenheimer, 1998; Pritchard
et al., 2012; Rignot & Jacobs, 2002). In the WAP, heat delivery from the
CDW has led in the past decade to an 0.68°C warming of the upper 300 m
of shelf water (Ducklow et al., 2007). In contrast, in the continental Antarctic
6
Chapter I. General introduction
most of the effects of the recent surface air global warming may have been
buffered by the presence of the stratospheric ozone hole (Turner et al.,
2013). By the end of the 21st Century the ozone above the Antarctic is
predicted to recover, and the influence of the increasing greenhouse gas
concentrations will likely be more important across Antarctica, with
potentially higher surface temperatures and drastic decreases in sea ice
extent (Turner et al., 2009, 2013), as is being seen today in the Arctic.
Nevertheless, these yearly-decadal climatic variabilities and their influence
on the Antarctic climate are yet to be totally understood.
The extreme seasonality of Antarctica (e.g. in light, weather and
temperature) is particularly evident in the extent of sea ice. The area
covered by sea ice increases from around 3–4 x 106 km2 in the austral
summer to 18–20 x 106 km2 in winter (Gloersen et al., 1992) with most of the
Southern Ocean biological primary production also taking place within this
region. The atmospheric and oceanic changes observed in the past
decades (e.g. positive phase of the SAM) seem to have influenced sea ice
cover in the Antarctic. In the WAP region, sea ice extent has dramatically
reduced, and the length of the sea ice ‘season’ has also shortened by
around 100 days (Ducklow et al., 2013) whereas, in the Ross Sea region,
the sea ice maximum annual cover area has increased and its season
extended (Lieser et al., 2013 and references therein). Overall, the maximum
annual extent of Antarctic sea ice has increased by around 285,000 km 2
(Cavalieri and Parkinson, 2008).
The rising temperatures and the intrusion of warmer deep waters have
initiated several regionally distinct responses from the Antarctic ice sheets
(Joughin et al., 2012). In the WAP extensive glacier retreat has taken place,
with 87% of glaciers retreating in the period 1953-2004 (see Fig 4, Cook et
al., 2005). Both sides of the Antarctic Peninsula have experienced ice shelf
collapse since as early as the 1970’s (George VI 1974-1995, Larsen A 1995,
Wilkins 1998, Larsen B 2002, Scambos et al., 2000, 2004), events which
subsequently accelerated flow rates in the tributary glaciers which fed
sections of the collapsed ice-shelves (De Angelis and Skvarca, 2003). The
increases in glacier retreat can be coupled during the austral summer
months to intense glacial discharge (e.g. glacial melt waters), snow and
permafrost melting which, in turn, affect coastal water turbidity and stability
(Dierssen et al., 2002; Vogt & Braun, 2004). Sea ice retreat, increased
meltwater discharge and the changes in atmospheric circulation with the
related variations in rainfall, have all been linked as the possible causes of
the freshening recorded in the past decades for the Antarctic waters (shelf
Ross Sea – 0.03 PSU decade-1 during the period 1958-2008, Jacobs and
Giulivi, 2010; N-W Weddel Sea shallow continental shelf – 0.09 PSU in 19897
Chapter I. General introduction
2006, Hellmer et al., 2011). Although these climatic responses appear very
dramatic for an ecosystem considered to be extreme but stable, some of
the changes (e.g. air temperature changes) that have occurred during the
instrumental record period (since 1950) in the Antarctic Peninsula seem to
fall within the natural climate variability range of this region, although they
represent rapid (but not unprecedented) rates compared to the climatic
fluctuations of the past 300-2000 years (Mulvaney et al., 2012; Steig et al.,
2013; Thomas et al., 2013) and processes may be different than those
which drove changes in the past.
Fig. 3 Antarctic near-surface temperature trends (1951-2006) based on station data,
a minimum of 35 years of data was required for inclusion. Abbreviations: AUT=
autumn; WIN= winter; SPR= spring; SUM=summer; MAM= March-April-May; JJA=
June-July-August; SON= September-October-November; DJF= December-JanuaryFebruary. From the SCAR “Antarctic Climate Change and the Environment” report
(Turner et al., 2009).
8
Chapter I. General introduction
Fig. 4 Summarized changes in glacier fronts since the earliest records to early 2000
(adjusted from Cook et al., 2005). Of 244 glaciers, 212 (87%) showed overall retreat
from their earliest known position.
2.2. Biological responses to climate change in Antarctic
coastal systems
The benthos: a quick general introduction
The benthos (from greek βένϑος "abyss”) includes highly interlinked
assemblages of metazoans (from greek μετά “change”, and zōia “animals”)
(Dahms et al., 2004; Maria et al., 2011a; Olaffson, 2003) which inhabit (or
live in close contact with) marine bottoms and interact with the microbiota.
The study of benthos (as for plankton) is carried out following a size class
subdivsion: i) the macrobenthos (from greek µάκρος "large" ) is composed
by those benthic organisms retained on a sieve of 1 mm mesh size; ii) the
meiobenthos (from the Greek μειός “to make smaller”) are organisms which
pass through a sieve of 1 mm mesh size and are retained on one of 0.032
mm, and, finally, iii) the microbenthos (from greek µικρος “small”) is
represented by those organisms, mostly unicellular prokaryotes and small
eukaryotes (protozoans), which are in the order of few tens of micrometers
in diameter. When looking at the metazoans realm, the above mentioned
size class subdivision reflects important evolutionary and ecological
divergences (or convergences) among the meiofauna and the macrofauna
(for some details on the different ecologies see Table 1). The macrobenthos
9
Chapter I. General introduction
is represented in the ocean by a multitude of vagile and sessile forms,
mostly belonging to the Anellida (e.g. polychaete worms), Cnidaria (e.g.
corals and sea pens), Mollusca (e.g. bivalves), Echinodermata (star fishes
and sea urchins), Porifera (e.g sponges), Tunicata (e.g. ascidians) and
Crustacea (e.g. amphipods and isopods).
Table 1 Biological characteristics of meiobenthos versus macrobenthos ( by Warwick
1984, in Giere 2009)
Animal weigth
< 45 µg
> 45 µg
Development
Direct, all benthic
With planktonic stage
Dispersal
Mainly as adults
As planktonic larvae
Generation time Less than 1 year
More than 1 year
Reproduction
Mostly semelparous*
Mostly iteroparous**
Growth
Attain an asymptotic final size
Trophic type
Often
feeders
Mobility
Motile
selective
Life-long permanent growth
particle Often non-selective
feeder
particle
Also sedentary
*Semelparous = with one single reproductive episode before death
** Iteroparous = with more than one reproductive episode before death
When considering the soft sediment communities and, more precisely, the
inbenthic macrofauna, the most common and abundant taxa are
polychaetes, amphipods and isopods, priapulids and bivalves. The density,
biomass and diversity of these soft sediment assemblages can be very
high, with up to hundreds of thousands of individuals per square meter
making up to hundreds of grams of ash free dry weight biomass (AFDW),
and being represented by up to hundreds of different species found in one
individual sampling effort (Heip et al., 1992; Van Hoey et al., 2004; Kędra et
al., 2010; Kowalke and Abele, 1998; Labrune et al., 2008; Siciński et al.,
2011; Ysebaert et al., 2003). Usually these communities are represented on
average by densities in the order of thousands of ind. m -2 making up to 1-10
g AFDW biomass.
The meiobenthos represents a very interesting biological compartment of
the eucaryotic realm, since it is composed by both multicellular metazoans
and unicellular protists. In this study we will focus mainly on the metazoan
component of this size class, leaving aside ciliates, foraminifera and
amoebozoans. Nearly all of the 38 metazoans major lineages have
10
Chapter I. General introduction
meiofaunal representatives (see Fig. 5) which had undergone the
evolutionary process of miniaturization (meaning "becoming smaller",
Rundell and Leander, 2010). Some of these animals belong strictly to the
meiofauna size class (e.g. gastrotrichs, gnatostomulids, loriciferans,
kynorinchs) and hence are ancestrally miniaturized, others have evolved
from macroscopic ancestors (e.g. anellids, arthropods, priapulids,
nemerteans). Some taxa are part of the "permanent" meiofauna since they
live their complete life-cycle into the meiofauna size class, whereas other
taxa (the " temporary" meiofauna) are in fact the juvenile or larval forms of
the local macrobenthic counterparts (Giere, 2009).
Fig. 5 Illustration showing the phylogenetic distribution of meiofauna lineages within
the Metazoa. Top left, the position of the Metazoa within the context of the tree of the
eukaryotes. (from Rundell and Leander, 2010).
The meiofauna is usually numerically dominated by the diverse group of
marine free-living nematodes (estimated in the order of 1 million existing
species), followed by harpacticoid copepods (and their larvae) and
polychaetes, although relative abundances and dominant taxa vary in
relation to the environmental specificities. The density, biomass and
diversity of the meiofauna in sediments can be as well very high, with
number exceeding the tens of thousands of organisms making up grams of
carbon equivalent biomass per ten centimeter square, with usually tens of
11
Chapter I. General introduction
taxa (higher taxonomical level) being present in each study site (Baguley et
al., 2008; Chen et al., 1999; Kotwicki et al., 2005; Leonardis et al., 2008;
Mascart et al., 2013; Tietjen, 1969; Vanhove et al., 2000; Varella Petti et al.,
2006). Most studies of meiofauna community composition are carried out at
the higher taxonomical level, only seldomly reaching the species level
detail, in light of the time consuming characteristic of such identification
work.
Meiofauna and macrofauna share the same environment (the sediment and
its interstices), but their diverging size spectra allow them to occupy
ecological niches that differ enough to avoid direct competition by
predation. Most permanent meiofauna goes through a direct development,
whereas most benthic organisms presents a plankonic larval stage which
often settles in the sediment once reached an average size beyond the
main prey size of meiofauna, thus avoiding the above mentioned direct
competition (Giere, 2009). Both size classes have evolved similar life styles
(interstitial, borrouwing, epibenthic etc.), feeding behaviours (deposit
feeding, predation etc.) but remarkably show rather different life history
modes. Generation times (GT) are usually faster in the small meiobenthos.
Most meiobenthic sized organisms complete a life cycle in less than one
year with a guess of maximum three generatios per year (Gerlach, 1971),
whereas macrobenthic organisms are told to have GT longer than a year
with variable number of generations per year, depending on the taxonomic
group or in light of species-specific adaptations (Sarà, 1984). Meiofauna
and macrofauna are highly interactive since they can prey (macrofauna on
meiofauna) or be preyed upon (meiofauna by macrofauna) one on/from the
other, either by direct feeding (selective meiofauna sized predation) or by
bulk ingestion of sediment (by macrobenthic deposit feeders) (Coull, 1999).
They are both tightly linked to, dependent on and responsible for the
biogeochemical characteristics of their environment. In marine ecosystems
meiobenthic and macrobenthic organisms (i) play a vital role in benthicpelagic coupling and the carbon cycle (Pape et al., 2013 ; Smith et al.,
2006; Tatián et al., 2008), (ii) stimulate the bioremineralisation (e.g.
denitrification) of detrital organic matter (via sediment bioturbation and/or
bioirrigation) (Bonaglia et al., 2014; Braeckman et al., 2010; Coull, 1999;
Nascimento, 2010), and (iii) may act as top-down control on the prokaryotic
sediment communities involved in the remineralisation process (Giere 2009
and references therein; Näslund et al., 2010). Benthic organisms interact
with the water column and sediment processes by means of a variety of
feeding strategies (e.g. filter-feeding and deposit-feeding) (Birkeland, 2012;
Buffan-Dubau and Carman, 2000; Fauchald et al., 1979; Pape et al., 2013;
Rosenberg, 2001; Tatián et al., 2002, 2007)), the fine-tuning of life cycle
12
Chapter I. General introduction
patterns (Marcus & Boero, 1998) and the evolution of taxon-specific
functional traits (Coull, 1999; Palmer, 1988).
The Antarctic benthos and its responses to climate change
The Antarctic marine macrofauna has long been remarked as showing a
more than passing resemblance to Palaeozoic assemblages (Aronson and
Blake, 2001; Dell, 1972). In fact, Antarctic shelf communities are dominated
by large biomasses of suspension and filter feeders (such as sponges,
ascidians, crinoids and ophiuroids) and almost totally lack the predative
pressure of modern skeleton-crushing (durophagous) organisms (such as
teleosts, elasmobranchs and decapods), the latter a feature that
characterized marine assemblages during the Paelaeozoic era. (Arntz et al.,
1994; Aronson et al., 2007; Brandt, 1999, 2005; Clarke et al., 2004).
Predative pressure is low on Antarctic shelves when compared to
temperate regions. Top predators are mostly represented by slow-moving
asteroids and nemerteans, which predate on the dense populations of
invertebrates, among which highly diverse groups include polychaetes,
bryozoans, sponges and amphipods (De Broyer et al., 2014; Clarke and
Johnston, 2003; Griffiths, 2010). Where ice scour impact is low (below 30-50
m) the sea floor can be fully covered by impressive three dimensional
assemblages of epibenthic filter and suspension feeders (Arntz et al., 1997;
Aronson and Blake, 2001; Clarke et al., 2004; Gili et al., 2006), with high
year-round biomass (Griffiths 2010; Smith et al., 2006). In recent decades
the Antarctic macrobenthos has been the focus of intense and widespread
scientific investigation (e.g. Arntz et al., 1997; Aronson and Blake,
2001;Brown et al., 2004; Clarke et al., 2004; Echeverría and Paiva, 2006;
Gili et al., 2006; Griffiths, 2010; Gutt, 2001; Mincks and Smith, 2006; Norkko
et al., 2007; Sañé et al., 2012; Siciński et al., 2011; Smale, 2008). In
contrast, the Antarctic meiofauna remain very poorly studied (see Table 2
for a general overview on Antarctic meiofauna investigations relevant to this
thesis work). From the available literature it appears that this small-sized
benthic class is represented in the Antarctic by often high abundance and
biomass, and comparably high taxon diversity to that found in other
temperate regions (Siciński et al., 2011; Skowronski & Corbisier, 2002;
Vanhove et al., 2000; Veit-köhler, 2005; Varella Petti et al., 2006; Veit-Köhler
& Fuentes, 2007).
On geological timescales, Antarctic shallow water benthic assemblages
have been shaped by the waxing and waning of the continental ice sheets
in response to various drivers, including orbital variations on Milankovitch
frequencies (Clarke and Crame, 2010). There is evidence that, during
13
Chapter I. General introduction
glacial maxima, grounded ice did not cover all areas of the continental
shelf, or synchronously, potentially allowing the existence of a mosaic of
refugia for the survival and allopatric speciation of benthic organisms
(Clarke et al., 2004; Convey et al., 2009b; Clarke & Crame, 2010). On
biological timescales, the duration, extent and seasonality of sea ice,
frequency of ice impact (e.g. ice scouring or anchor ice) and glacial
discharge dynamics deeply influence Antarctic coastal marine ecosystems
and can structure marine benthic communities (Brown and Milner, 2012;
Clarke et al., 2007; Gutt, 2001; Ileva-Makulec Krassimira and Grzegorz,
2009; Lee et al., 2001b; Quartino et al., 2013; Sahade et al., 2008; Vogt and
Braun, 2004)) in ways that are tightly linked to the synecology and life
history traits of the affected organism size classes. Sea ice extent and
advance/retreat variability have an indirect bottom-up control on benthic
communities, through tuning primary production and, hence, the timing and
quantity of the freshly produced organic matter available to benthic food
webs (Smith et al., 2006; Mendes et al., 2013). It has been reported that a
delay in sea-ice retreat could reduce phytoplanktonic primary producer
biomass (Mendes et al., 2013) and hence impact regional food web
interactions. During glacier retreat and/or ice shelf collapse new ice-free
habitats are exposed from previously ice-covered areas. This allows
primary production to take place, increasing the overall local productivity
and the carbon sink effect (Peck et al., 2010) and favoring colonization of
the ice-free substrata (Gutt et al., 2011; Hauquier et al., 2011; Quartino et
al., 2013; Raes et al., 2010).
Colonization processes are tightly linked to organisms’ dispersal potential
and their capacity to colonise new areas and escape environments that
become inhospitable. The majority of meiofaunal taxa lack highly dispersing
planktonic larval stages but can be dispersed mainly as adults over short
distances via bottom currents after re-suspension in the water column (e.g.
during storms or if displaced by strong currents; Palmer, 1988). Thus they
may require more time to colonize new areas than do organisms with
pelagic planktonic larvae. Nematode communities, for instance, were
observed to colonize the newly ice-free Larsen B shelf area sediments as
result of a (relatively) slow successional process (Raes et al., 2010). VeitKöhler et al. (2008b) during an in situ experiment performed in the coastal
Arctic, observed that the colonisation of bare soft sediment containers by
meiofauna may took several years before the experimental units host a
meiobenthic assemblage comparable in terms of abundance and diversity
to that found in the surrounding ambient sediments. These observations
would suggest that meiofauna and especially nematodes colonization
potential is limited in time and space. Nevertheless, Lee et al. (2001b) and
14
Chapter I. General introduction
Peck et al., (1999) found that the majority of Antarctic shallow water
meiofauna taxa returned to the sediments of a fresh scour within 20-30 days
from the catastrophic event, with copepods, nauplii, nematodes and
ostracods being the pioneer colonizers. Interestingly, Danovaro et al. (2001,
2004) found that an anomalous drop in temperature of 0.4 °C in the deep
Eastern Mediterranean was sufficient to decrease the nematode
assemblage abundance and functional diversity, whereas an increase in
species richness was observed. The latter was possibly due to a long
distance migration of colder Atlantic deep-sea species (Danovaro et al.,
2001), whose settlement in the alloctonous sediments was favoured by the
overall decrease in density of the affected local nematode assemblage.
Accordingly, Boeckner et al. (2008) concluded from an in situ experiment
that even very weak currents can be sufficient to suspend and transport
meiofaunal organisms, and that many of them are capable of active
dispersal into the water column. Another study in the deep Arctic
investigated the coupled effect of various azoic sediment types (e.g. deepsea-like sediment, sand, glass beats) and food (algae, fish, yeast) on the
colonization patterns of meiofauna, finding that different taxa were most
successful in different treatments (e.g. foraminifera in deep-sea-like
sediment treatments and harpacticoids in sand sediment treatments;
Freese et al., 2012). From these evidences it appears that colonization by
meiofauna varies in relation to local conditions (waves, currents, sediment
type and food availability) and species- and assemblage-specific
adaptation to the local natural disturbance types and that in high energy
environments its potential for the colonization of new habitats is likely higher
than in more stable environments.
Alternatively, some Antarctic macrofauna display high larval dispersal
potential (with long-lived and actively feeding pelagic larvae) and can
readily colonize scoured areas or newly available space by locomotion or
via dispersal (Poulin et al., 2002). Peck et al. (1999b) observed in Antarctic
after ice-scour soft sediment the early (after only 10 days) colonization by
motile organisms such as the serolid isopod Paraserolis polita or other
amphipods. A big storm after more than three months time enabled the
recolonisation of the sediments by the small bivalve filter feeder Mysella
charchoti via wave resuspension. Therefore on a short time scale motility or
potential for passive dispersal act as main drivers in the macrobenthic
recolonization process. On longer time scale we may expect that life-history
traits such as timing and potential (survival time in the water column) of
larval dispersal, generation time together with species-specific
physiological characteristics will influence the fate of macrobenthic
assemblages in a rapidly changing Antarctic.
15
Chapter I. General introduction
Intense glacial discharge can dramatically alter water column turbidity,
salinity and stability (Dierssen et al., 2002), at least locally and in a punctual
fashion (e.g. during summer months). The changes in the water column
properties affect directly the primary production efficiency (e.g. via shading;
Schloss et al., 2002) and may cause regime shifts in phytoplanktonic
assemblages when fresher and colder meltwater stabilises the water
column and larger diatoms are then replaced by smaller cryptophytes
(Moline et al., 2004; Mendes et al., 2013). These community shifts can
ultimately cause trophic cascade effects on the food web (e.g. a shift from
krill to salps; Moline et al., 2004). Nevertheless, melt waters can also
introduce large amounts of nutrients locally, stimulating primary production
(Dierssen et al., 2002) that subsequently becomes available for the
benthos. Grange and Smith (2013) defined Antarctic fjords as hot spots of
megafaunal biodiversity when compared to the less disturbed open shelf. In
the fjords, local weak inputs of meltwater promote primary production and
stabilize the water column without increasing the turbidity, and macroalgal
detritus is abundant and represents a major carbon source that is lacking
on the wider shelf. These authors concluded that increases in the intensity
of melt water discharge may pose a serious threat to the contemporary
Antarctic fjord biodiversity. Furthermore, intense glacier calving increases
the frequency of ice growler formation and ice scouring, events that are
known to influence the bathymetric distribution and local diversity of coastal
Antarctic benthos, with higher abundance and diversity found in deeper
and less affected waters (Smale et al., 2008; Smale, 2007, 2008; Varella
Petti et al., 2006). In such a complex environmental context, the
investigation of assemblages with differences in size spectra, development,
generation time, dispersal and re-colonisation potential, will make an
important contribution to understanding of the possible responses that the
West Antarctic Peninsula (WAP) benthos may display towards
contemporary and ongoing climate and environmental changes.
When investigating biological responses to climate change, it is of
fundamental importance to establish a sound baseline on the present (and
past when possible) benthic community distribution and structure at
sites/regions of ecological relevance and with contrasting characteristics in
relation to the ongoing environmental changes (e.g. coves interested by
glacier retreat versus coves where the retreat is not happening yet or WAP
versus more continental Antarctic). This could be achieved by means of
long-term monitoring to be coupled to experimental studies on key-species
or key benthic groups focusing on parameters of interest (e.g. increased
inorganic sedimentation, temperature rise effect, water acidification effect
etc.). In the West Antarctic Peninsula only one published study by Barnes
16
Chapter I. General introduction
and Souster (2011) has benefited of a long-term (over 25 years) dataset
comprising fast ice duration, ice scour and one macrobenthic species (the
bryozoan Fenestrulina rugula) mortality at Rothera station, which allowed to
draw preliminary conclusions on the effects of increased iceberg scouring
on coastal benthos regional biodiversity. A dataset more punctual in time
but uncommonly extended in area for investigations in the WAP (it
comprised 7 stations within the the Palmer Long Term Ecosystem Research
- PAL-LTER - area, covering about 62 - 68° S latitude) is the one resumed
by Smith et al. (2012). Within the FOODBANCS project (part I and part II),
the authors integrated 15 months evaluation on WAP shelf benthic
ecosystem functioning (including standing stocks, respiration, spawning,
recruitment of the macro- and megabenthos) to conclude that some
ecosystem parameters may be resilient to climate-induced changes in
pelagic-benthic coupling (e.g. changes in sea ice duration and its influence
on the primary production), whilst many others would be sensitive to the
changes and respond in a yet non-linear fashion. On an even shorter
temporal and spatial scale Siciński et al. (2012) compared the
macroinbenthic communities of two glacial coves in Admirality Bay (King
George Island, WAP) to two undisturbed sites, finding strong influences of
the glacial melt streams and related inorganic load on the community
structure and overall diversity. These studies have focused on the macroand megabenthic assemblages only. No study to date have investigated
West Antarctic meiofauna in the context of climate change effects. Ingels et
al. (2012) made a synthesis of possible global environmental changes on
five major taxa of the Antarctic benthos, covering as well the most dominant
meiobenthic taxon, the Nematoda. During their compilation, the authors had
to search for information outside the Antarctic literature and often they had
to extrapolate possible responses to globally changing parameters from
experimental studies more than from in field surveys. This highlights the
scarcity of such investigations on Southern Ocean meiofauna. Ingels et al.
(2012) reviewed nematodes responses to climate change-related variations
in i) food quality and quantity, ii) sea water temperatures (expected
increase), iii) ocean pH (expected acidification) and iv) sea ice dynamics.
In general, nematodes seem to be relatively resilient (overall densities are
barely affected) to changes in all these parameters in light of the taxon high
turn-over rates, high trophic flexibility (non-selective deposit feeders are
usually the most dominant trophic group) and capacity to colonise post icesour sediments as well as newly ice-free habitats (Ingels et al., 2012 and
references therein). Nevertheless, community diversity and structure
(species or trophic evenness) can be affected by most of these
environmental changes, rising questions about the overall long-term effects
of climate change on the benthic ecosystem functioning.
17
Chapter I. General introduction
All these observations and conclusions on the effects of environmental
variability on the biota have to be put into an evolutionary perspective prior
to undoubtedly adduce such observations to the direct effects of climate
change. Environmental variability has selected and structured the marine
benthic communities along different time scales in the Antarctic. On a
geological time scale (millions of years), the Antarctic benthos has evolved
from a Mesozoic fauna, inhabiting a much warmer, ice-free environment, to
another selected to thrive in an ecosystem dominated by a continental ice
sheet, cool and relatively stable sea water temperatures and where the
marine environment energy fluxes are dominated by strong seasonality in
sea ice dynamics (Clarke et al., 2007 and references therein). Within the
current interglacial period (the Holocene) which happens to be the most
climatically stable period of the Earth’s history, the Antarctic benthos has
been selected to cope with the interannual variability in sea ice and ocean
that characterize its marine environment. Among the processes involved in
these fluctuations worth mentioning are the widely-known atmospheric
variabilities of El Niño Southern Oscillation (ENSO) – and related La Niña and the Southern ocean Annular Mode (SAM), which are dominant patterns
acting on a decadal to sub-decadal time scale and having, at least for the
ENSO teleconnections, world-wide effects (Marshall, 2007; Meredith et al.,
2004; Schneider and Steig, 2008; Turner et al., 2013a, 2013b). These large
scale processes seem to have effects on the sea ice dynamics, rainfall
(Turner, 2004) and recruitment and growth of marine organisms (Clarke et
al., 2007 and references therein). Nevertheless, although organisms may be
adapted to cope with historical levels of this variability, it does not mean
they would easily cope with significant increases in their frequency. The
Fourth Assessment Report of the IPCC (Solomon et al., 2007) averaged the
results of about 20 different climate models with historical changes run to
natural and anthropogenic forcing to simulate the 20 th century climate. From
this integration, it appeared that much of the observed change in
temperatures in the Antarctic may be due to natural variability, but
nevertheless some of the observed changes may have an anthropogenic
origin (Chapman and Walsh, 2007). Therefore, processes may be different
now compared to the past, and what will be the effects of human made
global warming on the natural climatic fluctuations is still difficult to predict
(Turner, 2004). In coming future species may find themselves to cope with
gradients of environmental change far beyond those experienced in their
recent evolutionary history, and how will they respond to that is yet difficult
to predict. To disentangle natural variability from climate change forcing,
future studies need to merge high quality information from the present and
past. Investigations on benthic community diversity and distribution from
both palaeoecological studies and ongoing long-term surveys have to be
18
Chapter I. General introduction
thoroughly investigated in order to find common patterns in relation to the
observed and estimated climatic variability of the present, historical and
geological past of the Antarctic environment.
19
Chapter I. General introduction
Table 2 Overview of most relevant literature on Antarctic meiofauna and the main highlights. Abbreviations: WAP = West Antarctic
Peninsula; ind. 10 cm-2 = number of individuals per 10 cm2 ; TOM = total organic matter: C/N = carbon to nitrogen ratio.
Area
1
2
3
Title
WAP Shallow
waters King George
Island
The Community Structure of
Meiofauna in Marian Cove,
King George Island,
Antarctica
WAP Shallow
waters King George
Island
Meiofauna study in the Potter
Cove - Sediment situation and
resource availability for small
crustaceans (Copepoda and
Peracarida)
WAP Shallow
waters King George
Island
Time period
MarchDecember
2007
Assemblage generalities
Main highlights
Low densitites (123-874 ind. 10 cm2
)
Study on Peracarida and
Harpacticoida
No correlation between total
abundances and season (e.g.
summer melt water stream)
No correlations between
nematodes densities and
environmental parameters
Harpacticoid copepod species
correlate with certain
environmental parameters
Cumacea mostly present with
soft sediment
Peracarids: up to 30 ind. 10 cm-2
Amphipods related to high TOM
VeitKöhler,
1998
biovolume of harpacticoid
copepods was related more to
TOM than to the C/N ratio and
chloroplastic equivalents or even
grain size and depth
P. jubanyensis was strongly
connected to depth and to a
lesser extent to small grain sizes
S. (S.) praecipuus showed a
preference for sites with low
chloroplastic equivalent values
VeitKöhler,
2005
A total of 9 meiofauna taxa
Nematodes ( > 90%), Copepods
(3.18%)
Influence of biotic and abiotic
sediment factors on
abundance and biomass of
harpacticoid copepods in a
shallow Antarctic bay
February
1996
Reference
Hong et
al., 2011
Harpacticoids: up to 90 ind. 10 cm-2
February
1996
The distribution and biomass
contribution of the two species
Pseudotachidius jubanyensis and
Scottopsyllus (S.) praecipuus was
studied in detail
20
Chapter I. General introduction
Table 2 Continued
Area
Title
Time period
Assemblage generalities
Main highlights
Reference
Three species (Apistobranchus glacierae,
4
5
6
WAP Shallow
waters King
George
Island
Bathymetric distribution of
the meiofaunal
polychaetes in the
nearshore zone of Martel
Inlet, King George Island,
Antarctica
summer of
1991 and
1994
WAP Shallow
waters King
George
Island
Meiofauna distribution in
Martel Inlet, King George
Island (Antarctica):
sediment features versus
food availability
summer
1996/1997
and
1997/1998
WAP Shallow
waters Signy Island
A seasonally varying
biotope at Signy Island,
Antarctic: implications for
meiofaunal structure
Desntities 20 - 70 ind. 10
cm-2
A total of 1895
specimens in 17 families
were found
Meiofauna was
dominated by
nematodes (>60%),
followed by harpacticoid
copepods, nauplii and
polychaetes
Average densitites 3050
('96/97) and 4090
('97/'98) ind. 10 cm-2
Denstities 700 - 18 800
ind. 10 cm-2
April 1991 November
1992
Nematodes (>82%)
followed by harpacticoid
copepods, ostracods
and turbellarians were
the most abundant
Leitoscoloplos kerguelensis and
Ophryotrocha notialis), all belonging to
the temporary meiofauna, making up to
70% of the total meiofauna polychaete
fraction
Meiofaunal polychaetes showed similar
distributional patterns to those of the
macrofaunal polychaetes in the area
Sedimentary features main factor that
influences the community structure
No correlation with microphytobenthic
biomass
Meiofauna colonisation at 25 m depth for
granulometric reasons and higher stability
dur to lower iceberg scouring (information
taken from de Skowronski et al. 1998 *)
Variation in meiofauna densities and
structure mainly driven by organic matter
input and availability
no real correlation with water temperature
change which remain rather low
Varella Petti et
al., 2006
de
Skowronski
and Corbisier,
2002
Vanhove et
al., 2000
21
Chapter I. General introduction
Table 2 Continued
Area
Title
Time
period
Assemblage
generalities
summer: > 10 000
ind. 10 cm-2
winter: < 5000 ind.
10 cm-2
Main highlights
Reference
virtual lack of a "winter stop" with never
limiting food conditions in sediments
Dominance of epistrate feeders over nonselective deposit feeders (with switches in
between years)
28 nematode genera: Daptonema,
Aponema, Neochromadora, Sabatieria
Microlaimus and Chromadorita made up
>97%
average meiofauna
densities 4950 - 13
170 ind. 10 cm-2
Nematodes up to
90% total densities
7
WAP Shallow
waters Signy
Island
The metazoan meiofauna and its
biogeochemical environment: the
case of an Antarctic shallow water
environment
JanuaryFebruary
1994
Harpacticoid
copepods and
nauplii up to 11%
densities
Ostracods up to 22%
Higher abundance in the surface (0-2 cm)
layers
Aponema, Chromadorita, Diplolaimella,
Daptonema, Microlaimus, Neochromadora
constituted almost the entire community
Strong similarity to nematofauna from
temperate regions
Vanhove et
al., 1998
Epistratum and non-selective deposit
feeders dominated the nematode
assemblage
High standing stock, low diversity and steep
vertical profile in densitites likely related to
high sediment productivity and reductive
character of the sediment
22
Chapter I. General introduction
Table 2 Continued
Area
Title
Time period
Assemblage generalities
Nematodes dominate
community
8
WAP Shallow
waters Signy Island
Recolonisation of meiofauna
after catastrophic iceberg
scouring in shallow Antarctic
sediments
December
1993August 1994
Epistratum-feeders and nonselective deposit feeders
dominant predators/omnivore
and selctive deposit feeders
r-strategist community (in
controls and scour sediments)
Communities at different
recolonisation stages
9
10
Weddel Sea
- Shelf Kapp
Norvegia
WAP Shallow
waters Signy Island
Meiofauna response to
iceberg disturbance on the
Antarctic continental shelf at
Kapp Norvegia (Weddell
Sea)
Janurary March 1998
Community recovery
following catastrophic
iceberg impacts in a softsediment shallow-water site
at Signy Island, Antarctica
December
1993 August 194
A total of 20 taxa in between the
three stations
Nematode dominate the
densities
Control community high
densities comparable to other
results for Signy Island see
Vanhove et al., 1998
Main highlights
Return of major meiofauna
groups to background density
levels within 30 days
Pioneering colonisers :
Copepods, ostracods,
nematodes
Nematode community structure
not affected by ice scour -->
community well adapted to ice
disturbance
Meiofauna taxonomic diversity:
old scour > undisturbed > fresh
scour
Nematode abundance in old
scour recovered to background
levels
Nematodes community
compositon affected by scour:
decrease of selective deposit
feeders, Desmocolecina and
Leptolaimina most sensitive
groups
Wind-driven resuspension
advected nematodes, ostracods,
nauplii to 9 m depth site between
20 and 30 days after the impact
Reference
Lee et al.,
2001b
Lee et al.,
2001a
Peck et al.,
1999
23
Chapter I. General introduction
Table 2 Continued
Area
Title
Time period
Assemblage generalities
Main highlights
Reference
Meiofauna densities
reduced by 90% by the
scour
Nematodes most affected
by fresh scour reduction of
>98.5%
11
12
Drake Passage
- Abyssal plain
Weddel Sea Shelf - Larsen
Meiofauna communities
along an abyssal depth
gradient in the Drake
Passage
Response of nematode
communities after large-scale
ice-shelf collapse events in
the Antarctic Larsen area
ANDEEP-1
cruise ANT
XIX/3
summer
2007
2731 Ind. 10cm-2 at
2290m depth and 75 Ind.
10cm-2 at 3597m depth
Nematodes most
dominant taxon (84-94 %),
Harpacticoid copepods
followed (2-8 %)
Other important taxa
kinorhynchs, loriciferans,
tantulocarids, ostracods
and tardigrades
A total of 80 nematode
genera identified
General tendency of decreasing
abundances of metazoan
meiofauna with increasing depth
Not all taxa displayed this pattern
Gutzmann
et al., 2004
Standing stocks are higher than the
average found at similar depths in
other oceans
Precollapse, sub-ice communities
were impoverished and
characterized by low densities, low
diversity and high dominance of a
few taxa
Post-collapse recolonization of the
‘inner’ stations is believed to be a
long-time process
Raes et al.,
2010
24
Chapter I. General introduction
Table 2 Continued
Area
13
14
Title
Time period
Weddel Sea Shelf - Larsen
Characterisation of the
nematode community of a
low-activity cold seep in
the recently ice-shelf free
Larsen B area, Eastern
Antarctic Peninsula
ANT-XXIII/8
Polarstern
campaign in
2006–2007
WAP- Drake
Passage and
Bransfield
Strait
Carbon sources of
Antarctic nematodes as
revealed by natural carbon
isotope ratios and a pulsechase experiment
RV
Polarstern
EASIZ II
January March 1996
Assemblage generalities
Main highlights
Nematodes densities
ranged from 563.38 ±
244.04 ind 10 cm-2 and
3079.86 ± 531.80 ind 10
cm-2
Communities living close to the former
ice-shelf edge are believed to be at an
intermediate or late stage of
succession (dominance of
Microlaimus) whereas the innermost
site was the most impoverished
assemblage with dominance of
Halomonhystera (opportunistic genus)
Densities here were comparable with
those at other Antarctic stations,
whereas they were considerably
decreased at the inner stations
Densities in the seep
samples were high >2000
individuals 10 cm-2
Community characteristics shared with
cold-seep ecosystems world-wide
Below-surface maxima
δ13C from 21.97 ± 0.86 ‰ and 24.85 ±
1.89‰)
Nematode assemblage
dominated by one species
of the family
Monhysteridae,
Halomonhystera spp. (80 86% of the total
community)
Possible shift from oligotrophic precollapse conditions to a phytodetritusbased community with ice-shelf
collapse
Investigation of natural
carbon isotope ratios of
nematodes coupled to a
pulse chase experiment
Results suggest substantial selectivity
of some meiofauna for specific
components of the sedimenting
plankton
Reference
Hauquier
et al., 2011
Moens et
al., 2007
25
Chapter I. General introduction
Table 2 Continued
Area
Title
Time
period
Assemblage generalities
Nematode δ13C showed a
larger range, from –
34.6‰ to –19.3‰
Amphipods, –26.5 to –
22.9‰; harpacticoid
copepods, –29.4 to –
20.8‰; polychaetes, –
28.1 to –23.9‰; and
single values for
halacarid mites of –21.5‰
and for cumaceans of –
21.2‰
During the experiment
given organic carbon was
remineralized at a rate
11–20 mg C m–2 day–1
15
Weddel
Sea Abyssal
plain
Comparison of the
nematode fauna from
the Weddell Sea
Abyssal Plain with two
North Atlantic abyssal
sites
ANDEEP II
Cruise of
the FS
Polarstern
(ANTXIX/4) February April 2002
Comparison of WAP
(Weddel Sea) and North
Atlantic (NA) abyssal
plains
WAP showed higher
nematode densities
WAP shared 25 genera
with the other NA sites
Main highlights
Reference
13
C-depletion in lipids and a potential
contribution of chemoautotrophic
carbon in the diet of the abundant
genus Sabatieria
No lag between sedimentation and
mineralization; uptake by nematodes,
however, did show such a lag.
Nematodes contributed negligibly to
benthic carbon mineralization.
The nematode communities at the WAP
were dominated by
Thalassomonhystera and
Acantholaimus, which is comparable to
the NA abyssal plains.
No endemic genera for the Southern
Ocean were found
The higher abundance of the genera
Microlaimus and Dichromadora seems
to be typical for the Southern Ocean
deep-sea, and might be related to the
availability of fresh food
Sebastian et al., 2007
*Info from referenced literature within cited article which was not accessible online
26
Chapter I. General introduction
3.
International context
In light of the key role of the Southern Ocean in the global ocean system, it
is crucial that a sound baseline of information on Antarctic marine
biodiversity exists. In order to be able to predict possible structural and
functional responses of Antarctic marine ecosystems to contemporary
climate and environmental changes, information on the ability of organisms
to respond to changes in environmental parameters (e.g. temperature, pH,
food quality and quantity, ice cover, ice impact) and the ecological role of
biodiversity in the functioning of the Southern Ocean must be gathered. In
this context several research programmes have carried out a wide range of
scientific investigations in the past decade, and the work described in this
thesis builds on this foundation.
The BIANZO II project (Biodiversity of three representative groups of the
Antarctic Zoobenthos - Coping with Change), funded by the Belgian
Science Policy, investigated the biodiversity of three major Antarctic
zoobenthic taxa Nematoda (meiobenthos), Amphipoda (macrobenthos) and
Echinoidea (megabenthos). These groups are characterised by a high
diversity and include many of the well over 4000 Antarctic benthic species
described to date (Clarke & Johnston, 2003; De Broyer et al., 2014;
Griffiths, 2010) belong to these taxa. The area of investigation covered
mostly the deep sea and continental shelf areas, with particular attention
focused on the Larsen A and B ice shelf loss areas (Ingels et al., 2011).
BIANZO II was developed in two phases. The first phase (2007-2008)
investigated biodiversity patterns of selected taxa of Antarctic zoobenthos
and the causal processes coupling trophodynamic aspects of each of the
benthic groups, and their ability to cope with warming temperatures,
acidification and disintegration of ice shelves. The various publications and
results generated during the first phase of the BIANZO II project culminated
during the second phase (2009-2010) in a review paper on the global
effects of climate change on the three representative benthic taxa, with the
additional inclusion of the Foraminifera (Ingels et al., 2012).
In 2009 the IMCOAST project (Impact of climate induced glacial melting on
marine coastal systems of the West Antarctic Peninsula region,
www.imcoast.org ) was funded by the European Science Foundation and
the Fonds Wetenschappelijk Onderzoek (FWO), amongst other agencies.
The project investigated the west Antarctic Peninsula coastal areas of Potter
Cove (PC) and Admiralty Bay, located on the southern coast of King
George Island (KGI), South Shetlands Islands. The west Antarctic Peninsula
27
Chapter I. General introduction
(WAP) is the richest part of the Antarctic continent in terms of biodiversity
(Clarke & Johnston, 2003; De Broyer et al., 2014: Griffiths, 2010) and is one
of the fastest warming regions on Earth (Turner et al., 2005, 2009, 2013;
Vaughan et al., 2003), experiencing rapid changes in terms of ice duration
and extent (Ducklow et al., 2013), glacier retreat (Cook et al., 2005) and ice
sheet instability (Scambos et al., 2000). Although these changes currently
lie within the natural variability of the region (Mulvaney et al., 2012 ; Steig et
al., 2013; Thomas et al., 2013), larger changes are forecast to happen in
the future (Turner et al., 2013), and the WAP is a very important region in
which to investigate, unravel and monitor the effects of these climatic
changes on the resident benthic communities. The strategy of the IMCOAST
project was to combine different physico-hydrographical, sedimentological,
geochemical and biological proxies to reconstruct and model past, ongoing
and future system bias due to coastal sediment run-off in the KGI-WAP
coastal area. The work described within this thesis is placed within this
international and interdisciplinary framework, within the research topic of
working package 4 “Biological response to climate change”, and includes
investigation of possible glacier-retreat-related impacts (e.g. increased
sedimentation, ice scour, changes in carbon sources) on PC meiobenthos
(and macrobenthos) from a structural and functional perspective. The
scientific approach taken is outlined in Section 1.4 below.
The investigation of climate change effects on biological communities is not
a task which can be carried out in a short amount of time. It requires longterm datasets and monitoring of community structure and functioning on
timescales that can integrate and differentiate natural variability from direct
change consequences. Therefore, a continuation of the BIANZO II and
IMCOAST projects has been funded recently by the Belgian Science Policy
(BELSPO). The vERSO (v-Ecosystem Responses to global change: a
multiscale approach in the Southern Ocean) project’s goal is to assess the
impact of the main stressors driven by global change in two areas
differently affected by climate change (Potter Cove, (KGI, WAP) and Terre
Adélie, continental Antarctica) on benthic ecosystems, using an integrated
approach including representative taxa from different size classes of the
benthos (prokaryotes, nematodes, foraminiferans, amphipods and
echinoids). To reach this goal, research on connectivity and adaptation,
trophic ecology, sensitivity and resilience will be conducted and integrated
using ground-proofed predictive models. The vERSO research integrates
into the new SCAR (Scientific Committee on Antarctic Research) Scientific
Research Programs (Antarctic Thresholds - Ecosystem Resilience and
Adaptation, AnT-ERA, and State of the Antarctic Ecosystem, AnT-ECO) and
will contribute data, models and advice to science-policy interfaces,
28
Chapter I. General introduction
committees, treaties and protocols to which Belgium is committed, such as
the Antarctic Treaty Consultative Meeting on Environment Protection (ATCM
CEP), the Convention for the Conservation of Antarctic Marine Living
Resources (CCAMLR), and the Convention on Biodiversity (CBD), together
with direct contributions to the new Antarctic Environments Portal initiative
and the Antarctic Conservation Strategy.
4.
Thesis background and scientific approach
4.1. West Antarctic coastal ecosystems: a case study
The Western Antarctic Peninsula (WAP) is a maritime region of the Antarctic
which is changing very rapidly, as already outlined in the previous section
1.2.2 (Fig. 6). The climatic changes in the area have initiated conspicuous
glacier retreat and annexed water column processes (Dierssen, 2002;
Turner et al., 2013), while the calving of the glacier fronts may increase the
frequency of ice growler impact on the shallow bottoms (Barnes & Kaiser,
2007). The coastal primary production may be locally increased by the
contribution of the newly ice-free areas that arise from beneath the ice
(Peck et al., 2010). Nevertheless, the shortening of the sea ice season and
the observed changes in its dynamics had strong consequences in and off
shore the WAP (Ducklow et al., 2013; Stammerjohn et al., 2008)), with an
observed decline in surface Chl-a in the north section by 12% over the past
30 years (Montes-Hugo et al., 2009). Marine and terrestrial communities are
changing their distribution and structure in response to these changes
(Barnes and Kaiser, 2007; Clarke et al., 2007). King-George Island (KGI),
located in the South Shetland Island archipelago north-west of the AP, has a
small isolated icecap which is responding rapidly to the observed aerial
warming (Rückamp et al., 2011). On its southern coast a fjord-like
embayment, Potter Cove (PC), is experiencing strong environmental
changes (see details in the next section), and rapid glacier retreat has
influenced the cove since the 1950’s. Potter Cove’s marine ecosystem has
been studied during several international collaborative projects, Imcoast
being one of them, and the resulting data have been sustainably archived
(www.pangaea.de), and are available to future projects and environmental
assessment panels such as the IPCC. Therefore PC represents a very
interesting case study to be used to understand climate change in the AP
region as part of larger scale global processes. Moreover, meiofauna (and
endobenthic macrofauna) are as yet poorly studied in the cove (as in the
Antarctic in general), and the work described within this thesis represents
an important advance in knowledge of their ecology and likely responses to
the ongoing regional changes.
29
Chapter I. General introduction
Fig. 6 Schematic summary of environmental drivers of regional climate change in the
Antarctic Peninsula and their relations with the biota (primary producers and benthic
consumers). SST = sea surface temperatures; ENSO = El Niño Southern oscillation;
SAM = Southern Annular Mode; WC = water column; Δ = variation; Temp =
temperature. References and rationale to be found in the text.
4.2. Potter Cove, King George Island, West Antarctic
Peninsula
King George Island (KGI, 62° 02’ S, 58° 21’ W), is the largest island of the
South Shetland Islands archipelago. Located off the northern tip of the
Antarctic Peninsula (See Fig 7a), KGI has a maritime climate dominated by
north-westerly winds and summer temperatures which are frequently above
0°C (Schloss et al., 2012). KGI’s climate is further characterized by the
influence of large scale features such as the Southern Annular Mode (SAM)
and the El Niño Southern Oscillation (ENSO) (Bers et al., 2012). The recent
warming observed in this region since the 1960 s (see Table 3) is attributed
to a shift towards a positive phase of the SAM. Warming of mean summer
air temperatures of about 2°C in the past 50 years at Carlini (formerly
Jubany) Station in Potter Cove (Schloss et al., 2012), in the northern
Antarctic Peninsula region, is less pronounced than the warming that has
occurred in the more southern Antarctic Peninsula (2.5°C in the past
decade at Vernadsky-Faraday station, Turner et al., 2009, 2013). KGI is a
volcanic island of 1100 km2, of which 90% is ice covered, and whose
highest elevation reaches to 700 m a.s.l. (Osmanoğlu et al., 2013). Rapid
30
Chapter I. General introduction
melting of the KGI icecap and retreat of tidewater glaciers in the past 20
years have caused massive and visible changes (Fig. 7) to the island’s
landscape including newly ice-free areas on land and under water, and soil
erosion through surface and subterranean melt water run-off.
Potter Cove (PC, 62° 14’ S, 58° 42’ W ) is a fjord-like inlet on the southern
coast of KGI of about 4 km length (W-E) and 2.5 km width (N-S) (see Fig. 7
and Fig. 8). The cove can be divided into an inner part, presenting a
maximum depth of 50 m, and an outer cove where depths reach 100-200 m
(Klöser et al., 1994). The dominant bidirectional winds (E-W) generate a
cyclonic gyre with particle-free waters entering PC from Maxwell Bay along
its northern shore and export of sediment-laden waters from the south
(Roese and Drabble, 1998). Depending on the wind direction, downwelling
(westerly winds) or upwelling (easterly winds) can occur in the inner part of
the cove (Klöser et al., 1994). The eastern and northern coasts present
steep slopes covered by the Fourcade Glacier. This tidewater glacier has
been actively retreating (see Fig. 7b) since the early 1950s, and in the past
60 years several areas have become ice-free as the glacier front has almost
completely retreated onto the land (Fig. 7b). The southern coast (Potter
Peninsula) displays a rather flat topography and during the summer melting
period (October-March) glacial melt water streams (see Fig. 7c) drain
melting snow, permafrost and glacial ice (Eraso and Dominguez, 2007).
Despite the relatively high input of melt waters in the cove, no significant
trends in freshening of the inner cove have been reported for the past
decades. Schloss et al (2012) made an analysis of climatic trends for the
period 1991-2009 in Potter Cove. They showed no evident salinity trend
anomalies in neither the outer or inner cove during the studied period.
Among the possible drivers of the observed changes, ENSO did show
strong links with air temperatures, seas surface temperatures, sea surface
salinities, chl-a concentrations and total suspended particulate matter,
detectable both in the inner and in the outer cove (Bers et al., 2013).
The monthly salinity variation is more pronounced in the inner cove than in
the outer part of the bay and it is related to the creek formation during
summer months. Nevertheless, Schloss et al (2012) observed that this water
layer is exported out of the cove by the clock-wise current system and the
low salinity waters are not mixing with the deeper layers. In the inner cove
the salinity ranges from 33.4 PSU during the months of January and
February and it stabilizes around 34 PSU during the rest of the year
(Schloss et al., 2012). In light of the ongoing glacier calving during the
summer months, growlers are often present during the melting period and,
in light of the glacier front position and the clockwise circulation system, are
mostly found along the eastern and southern sides of the cove (pers. obs.;
31
Chapter I. General introduction
Philipp et al., 2011). Ice scour is common up to 20 m depth (Sahade et al.,
1998), leading to reduced diversity and biomass in the epibenthos.
In most of the inner cove and along the southern coast soft bottoms are the
typical substratum type, with coarser sand present in the areas of glacial
outwash stream discharge. Dispersed rocks and boulders may be remnants
of moraines deposited by the Fourcade Glacier. The north-eastern coast is
typified by rocky or rough substrata (Fig. 8, Wölfl et al., 2014).
Phytoplankton primary production (PP) in Potter Cove is usually low (<5 mg
Chla m-3; Schloss and Ferreyra, 2002; Schloss et al., 2002, 2012). Low PP in
the area is related to wind-induced turbulent mixing and seasonal light
limitation due to water turbidity (related to glacial ablation). Within the cove
a higher dominance of small phytoflagellates as compared to diatoms is
usually observed in the areas closer to the meltwater discharge of the Potter
Peninsula riverine system (García et al., under.rev.). Nevertheless, in
January 2010 the largest recorded, diatom dominated, bloom in the past 20
years (>20 mg Chla m-3) was observed and linked to the rather cool
summer temperatures and the dominant easterly winds during that summer
(Schloss et al., 2014). Given the usually low phytoplankton PP found in
these waters (Schloss et al., 2002, 2012; Schloss & Ferreyra, 2002),
macroalgal PP (up to 1,370.61 mega tons PP flux to the benthos in 19941995; Quartino & Boraso de Zaixso, 2008) has been suggested as the main
food source responsible for the high biomass of secondary consumers
present in PC.
Table 3 Aerial and surface water warming trends for the Potter Cove area (KGI)
based on data from Carlini Station and Servicio Metereologico Nacional of Argentina
(also Schloss et al., 2012)
Summer air T
Winter air T
Sea Surface T
warming per decade
50 years warming trend
+ 0.39° C
+ 0.48° C
+ 0.36° C
+ 2° C
+ 2.4°C
+ 1.8°C
32
Chapter I. General introduction
Fig. 7 Aerial overview map of Antarctica (http://www.map-of-antarctica.us) and King George Island (adapted from Rückamp et al.,
2011), its position in the west Antarctic Peninsula region and the location of Potter Cove (PC) in respect to Maxwell Bay (a) Potter
Cove map (b), showing glacier retreat since 1956 with the new ice-free areas indicated by blue lines (modified from Rückamp et
al., 2011) and Carlini Station (former Jubany) highlighted in the white circle. The retreat (advance) areas on KGI are indicated in
red (green). Ice front lines are given for both KGI and Potter Cove.
33
Chapter I. General introduction
Fig. 8 Sediment granulometry distribution within Potter Cove (from Wölfl et al., 2014).
Macroalgae require hard substrata on which to develop. In PC, until
recently, the seaweeds were mostly present in the outer cove (Quartino &
Boraso de Zaixso, 2008), but, with ongoing glacier retreat, more rocky
areas have become available in the inner cove (Fig. 7b, Fig. 9b) and these
newly available hard substrata have been colonized by seaweeds (Quartino
et al., 2013). This change is proposed to have significant implications for
the cove’s energy budget (Quartino et al., 2013). Another likely food source
for benthic organisms could be represented by sediment microalgae. To
date, microphytobenthos have been studied only in terms of diversity (AlHandal and Wulff, 2008) and no estimation of their primary production
contribution has been made in the cove. Nevertheless, benthic microalgae
have been observed to be an important food element for ascidian species,
along with macroalgal detritus (Tatián et al., 2002, 2004) and, during
summer months, dense microalgal mats can be observed on shallow soft
bottoms when stable (low wind) sea surface conditions are present for a
sufficient time (pers. observ.). When these mats are formed, tracks of grazer
organisms (e.g. amphipods) on the sediment surface are a clear sign that
this primary producers biomass can be utilized by higher trophic levels
(pers. observ.)
.
Potter Cove is affected by significant bed shear stress due to wave action,
especially near the northern and southern shores (Wölfl et al., 2014). Wave
disturbance can cause sediment resuspension and this can stimulate
34
Chapter I. General introduction
bacterial remineralisation (Pusceddu et al., 2005) of fresh detritus or make
this organic matter available to suspension feeders (Tatián et al., 2002,
2004). The benthic microbial communities in PC are likely to be very
important contributors to the overall energy fluxes. Although they have not
yet been investigated in terms of biomass or remineralisation potential,
these communities are known to be part of the so called “small food web” of
the world’s marine sediments (Giere 2009), and to be crucial in redirecting
detrital organic matter (e.g. macroalgal detritus) to higher trophic levels
(e.g. via feeding by bacterivorous organisms such as selective nematodes
or copepods (Giere, 2009; Rieper, 1982), or by being passively ingested by
non-selective deposit-feeding macrofauna).
Potter Cove macro-epibenthic communities are highly abundant and
diverse. Grange and Smith (2013) placed PC within those fjords that
represent biodiversity hotspots in the Antarctic. In the inner cove the
epibenthic assemblages present an evident bathymetric pattern, with
increasing diversity and abundance/biomass from 20 m towards deeper
waters (Sahade et al., 1998), thought to be caused by ice scour
disturbance at shallower depths. The epibenthic community has shown
changes in recent decades in terms of the relative dominance of sessile
species at different depths and areas within the cove (Sahade et al., in
prep), changes that have been related to species-specific tolerance to the
increased load of sediment-bearing glacial melt waters entering the cove
due to glacier retreat and the warming summer temperatures (Torre et al.,
2012, 2014).
Meiofauna and soft bottom infauna have been poorly studied in PC (Mayer
2000; Kowalke & Abele, 1998; Veit-Köhler, 1998, 2005; Veit-Köhler et al.,
2008). Meiofauna was studied by Veit-Köhler et al. (2008) along a depth
profile from the Potter Peninsula (southern coast) to the centre of the cove,
showing high abundances with a 20 m depth peak, which was suggested to
be due to the lower disturbance at depths deeper than 15 m. Harpacticoid
copepod assemblages have been investigated in relation to sediment biotic
and abiotic factors (Veit-Köhler, 2005) along three depth transects, and
showed no strong relation to depth but rather to sediment organic matter
content. No studies on meiobenthic nematode community composition have
been carried out in PC to date. Endobenthic macrofauna were sampled
along four transects from the entrance (Punta Elefante) to the inner part of
the cove along an S-N axis (Kowalke and Abele, 1998). Contrary to the
observations on meio- and mega-epibenthos, the endobenthic soft bottom
macrofauna showed generally higher abundance at the shallower stations
(0-10 and 10-20 m) with a rather steep decline in deeper waters (~30 m)
35
Chapter I. General introduction
long transects closer to the cove entrance, whereas patterns in the inner
part of the cove were less pronounced.
a
b
c
Fig. 9 (a) Potter Cove view from off shore. The “three brothers hill” of the Potter
Peninsula (southern coast) is visible on the right. The red buildings are the containers
of Jubany/Carlini base. The nunatak present on the Fourcade glacier at the eastern
side of the cove is visible. (b) Glacier calving in the vicinity of one of the new ice-free
areas (dark rocky islands) on the northern shore. (c) Glacial riverine discharge of
Potter Creek along the Potter Peninsula in March 2010.
Relative abundances of dominant taxa showed the presence of
sedimentation-tolerant groups in the shallower and inner stations (e.g.
cumaceans). Therefore it appears that PC meiofauna and endobenthic
macrofauna present contrasting patterns of community structure along the
small depth gradient investigated so far (see Fig. 10). Part of the current
study sets out to relate the in situ assemblage structural and functional
characteristics to the local glacier retreat-related conditions (Chapter II and
Chapter III, meio- and macrobenthos) and to the seasonality of the region
(Chapter IV, only meiobenthos). Moreover, this research investigated the
effects of the glacial-related singular forcing on the meiobenthic
assemblage structure by means of laboratory experiments (Chapter VI).
36
Chapter I. General introduction
Fig. 10 Visual scheme of Potter Cove meio-, macro- and megabenthic fauna density
vertical patterns (non quantitative) in relation to the mainl driving environmental forces
(here graphically represented left to right: wave-related disturbance, ice growler
action and inorganic sedimentation). In this schematic view, the horizontal gradient
(e.g. inner versus outer cove) of these forces was not taken into account. Density
vertical profile data are extrapolated from Veit-Köhler (1998; for meiofauna), Kowalke
and Abele (1998; for soft sediment macrofauna) and Sahade et al. (1998, 2008; for
megabenthic fauna). The dashed areas represent hipotetical expected patterns not
yet investigated and hence supported by published literature. See text for further
detail.
4.3. Trophic structure at the community level: a stable
isotope approach
Life is characterised, as in the oceans as on land, by a flow of energy which
moves from the inorganic world to the world of living organisms and it is
then remixed, redistributed or exported via a series of trophic links, detrital
pathways, remineralisation processes and burial. A functioning ecosystem
can be oversimplified to a series of naturally fluctuating but relatively stable
links in between (and within) the environment and the organisms where
energy in the form of carbon is passed on from the atmosphere to the biota
through a series of complex trophic links and specific metabolic pathways.
In a rapidly changing context, Antarctic benthic metazoans are bound to
respond to the ongoing perturbations by modifying their interrelationships
with the environment and the other organisms. The popularity of stable
isotopes analyses to trace energy flow between food sources and
consumers has increased at a spectacular rate. Their potential in tracing
element fluxes has also proven to be a useful tool to analyse the structure
37
Chapter I. General introduction
and the overall functioning of marine communities. Understanding the
degree of trophic connectivity (the degree to which higher trophic levels
feed on different trophic levels) of either a population or an entire
ecosystem is of fundamental importance if we are to understand their
inherent stability and potential resilience to perturbations (Madigan et al.,
2012). In the context of this thesis work, stable isotopes (namely δ13C and
δ15N anlaysis, see further for details) appeared to be a valuable tool to
investigate the interactions of the benthic organisms in Potter Cove and
bring insights in the overall benthic assemblage stability and its potential
responses to future perturbations.
Stable isotopes represent a time-integrated imprint of an organism’s
interaction with its surrounding environment and therefore can widen the
knowledge of species synecology and assemblage relationships. Carbon
and nitrogen stable isotopes are the most common isotopes used in
ecological studies (Peterson and Fry, 1987). The rationale behind stable
isotope analysis is straightforward: in nature carbon ( 12C, light isotope and
13
C, heavy isotope) and nitrogen (14N light isotope, and 15N heavy isotope)
isotopes are present in constant (stable) ratios in the inorganic world, but
they are partitioned by organisms’ metabolic pathways. During assimilation
and respiration the lighter isotope is “metabolised” more easily as it is
lighter and, hence, from the inorganic world, to the primary producers and
up to the higher consumers the organisms become enriched in the heavier
isotope (Fig. 11). At each trophic step (or trophic fractionation, Δ), the value
of this ratio changes, reflecting the increasing proportion of the heavier
isotope (Fry, 2006). Isotope abundance in the animals’ tissues is noted in
the delta “δ” notation since the percentage of heavy isotope is measured
with respect to a known standard (PeeDee Belemnite for δ13C and air for
δ15N) and this notation has the advantage to “enlarge” the otherwise
extremely small (in the order of 1/1000) differences in the fractions of the
heavy isotope in between sources and consumers. This leads to a
straightforward linear means to relate to the percentage of the heavier
isotope: the larger the δ value, the higher the heavier isotope percentage in
the organism’s tissue (Fry, 2006). In food web studies, δ13C is generally
used as a source indicator as it changes from food source to consumer
(Δ13C = 0–1‰, DeNiro and Epstein, 1978; McCutchan et al., 2003) and it
can vary between different producers. For instance, water column
microalgae are known to display a significantly lighter carbon isotopic
signature compared to their benthic counterparts (on average with a
difference of 7‰, in light of the different diffusive properties of CO2 at the
sediment boundary-layer and the resulting decrease in overall fractionation
(Bouillon et al., 2011; France, 1995). The δ15N trophic fractionation (Δ15N) is
typically higher and it is considered to change Δ15N = +3‰ for each trophic
38
Chapter I. General introduction
link but with a large variation around their mean (McCutchan et al., 2003).
δ15N is mainly used to calculate relative trophic position of consumers in a
food web (Post, 2002). Hussey et al. (2014) argued that a constant trophic
fractionation is unrealistic and mostly a pragmatic assumption. They
demonstrated that trophic fractionation usually decreases with each trophic
step and the use of an additive framework (with a constant Δ15N) results in
truncated food web lengths where the overall number of trophic positions
(TPs) is underestimated. The authors suggest the use of species metaanalysis to find Δ15N versus δ15N dietary relationships to estimate consumer
trophic position using an δ15N-dependent enrichment model which allows to
narrow Δ15N values with increasing dietary δ15N. This approach results in a
scaled food web where apex predators occupy higher TP s than they would
by means of a constant trophic fractionation step (Hussey et al., 2014). This
method has important consequences for the estimation of energy flow
through a specific length food web knowing that biomass transfer efficiency
between trophic steps is roughly only 10% (Lindeman, 1942). McCutchan et
al. (2003) found that fractionation steps differed based on the diet of
organisms: i) an average δ15N trophic fractionation of 1.4 ± 0.21‰ was
associated with food-webs mostly based on invertebrate diet; ii) an average
δ15N trophic fractionation of 2.2 ± 0.30‰ was found for organisms fed with
plant and algal diets and finally iii) an average δ15N trophic fractionation of
3.3 ± 0.26‰ was found to be characteristics for high protein diets.
Fig. 11 Expected increase in
δ13C (indication of food
source) δ15N (indication of
trophic position) in a typical
marine food web.
In combination with δ13C, δ15N can give information on the diet since it may
differ between sources (Vander Zanden and Rasmussen, 1999). Carbon
and nitrogen stable isotope analysis in the Antarctic have been used to infer
39
Chapter I. General introduction
dietary information for benthic organisms, providing broad inferences
based on relative isotope values of consumer and resources, initially
resulting in descriptive outcomes (Corbisier et al., 2004b; Dunton, 2001;
Gillies et al., 2013, 2012; Kaehler et al., 2000; Pakhomov et al., 2004). Over
the past decade several more quantitative approaches have been
developed and, in the most recent works on Antarctic food webs, they have
been used to generate inferences about food-chain length and to
schematise organic matter fluxes (Gillies et al., 2012, 2013). To investigate
the whole range of resources (bionomic niche axes) exploited by a
population can be very difficult. A more measurable concept in ecology is
the feeding niche (or trophic niche), which Elton (1927) defined as the
dietary diversity of an animal. The isotopic δ-space (δ13C versus δ15N plot)
occupied by an animal or population can therefore provide a representation
of the niche of a population given a specific resource pool, as an animal’s
chemical composition reflects what it consumes (bionomic). Among the
most novel approaches (see Table 4), community-wide metrics have been
proposed as a valuable method to estimate community isotopic niches, as a
time-integrated parallel to the population trophic niche. Layman et al. (2007)
proposed six metrics (see Chapter III) where mean carbon and nitrogen
isotope values of consumers are used to measure several aspects of
trophic diversity and make inference about trophic redundancy of biological
communities. Four of these metrics describe the community-wide trophic
diversity: i) TA (total area) is a convex hull area encompassed by all the
individuals in the δ13C-δ15N bi-plot space and it gives a measure of the total
extent of trophic diversity in a food-web; ii) CR (δ13C range) measure the
distance between the two species with the most enriched and the most
depleted δ13C values, giving a measure of niche diversification at the base
of a food web (e.g. higher CR means more diversified source pool); iii) NR
(δ15N range) measure the distance between the two species with the most
enriched and the most depleted δ15N values, giving a visual measure of the
vertical structure of a community (how many trophic levels are there); iv) CD
(mean distance to centroid) is the mean of the Euclidean distances of each
species to the δ13C-δ15N bi-plot centroid (mean value for all species in the
bi-plot space), it gives a measure of the average trophic diversity within a
food web.
The last two metrics deal with the level of trophic redundancy within a food
web and they calculate it as a measure of species packing within the bi-plot
space: i) NND (nearest neighbour distance) is calculated as the mean of
the Euclidean distances of each species to their nearest neighbour in the
bi-plot space, it gives a measure of the density of species packing; ii)
SDNND (standard deviation NND) it’s a measure of the evenness of species
40
Chapter I. General introduction
packing. Food web length, trophic niche diversification, total amount of
niche space and trophic redundancy are features which can be compared
between different populations (or for the same population at different time
periods) and highlight possible environmental influences on the
organisation of biological communities (Abrantes et al., 2014; Layman et al.,
2007), given that a standardised baseline has been considered when
comparing different communities/ecosystems (Post, 2002). Nevertheless,
these metrics have been found to be biased by the quality of the dataset
under study, and especially to be suffering with sample size (number of
points or species in the isotopic biplot) of n < 10. Jackson et al. (2011)
integrated a Bayesian based statistical approach to these metrics in order
to take into account the uncertainty in the sampled data propagating
throughout the measures the error inherent to the sampling process (e.g.
unbalanced datasets to be compared). They developed a novel multivariate
ellipse-based metric (Standard Ellipse Area or SEA) as an alternative to the
convex hull areas which proves to be less biased by small sample size, a
usual limitation for the often small datasets available in otherwise expensive
food web studies.
Fig. 12 From Jackson et al. (2011). Comparison of Convex Hulls (solid black lines)
and Standard Ellipse Areas (circles) calculated from the same population (open
circles) for (a) n = 10 and (b) n = 200. The true population standard ellipse for the
two examples is a circle with radius = 1.
The standard ellipse areas (SEAs) are to the δ13C-δ15N bivariate dataset
what a SD is to a univariate dataset. Of a bivariate isotopic dataset, the
SEAs represents its true distribution. The ellipse shape is given by the
dataset associated covariance matrix whereas its location is defined by the
means of the bivariate isotopic data (Jackson et al., 2011). Standard Ellipse
Areas are a straight forward way to gain information on the trophic variability
41
Chapter I. General introduction
within and between food webs integrating uncertainty and the ineherent
variability of the data (see Fig. 12).
42
Chapter I. General introduction
Table 3 Summary of characteristics of the community-wide metrics vs Standar Ellipse Areas (SEAs)
What
Community-wide metrics
(Layman et al., 2007)
Metrics used to quantify the
area (as convex hulls) of an
isotopic (δ13C and δ15N)
bivariate space
Applicability
They provide visually straight
forward and detailed
information on population's
trophic structure by means of
community-wide measures of
trophic diversity and
estimations of trophic
redundancy extent
Pros
•They do not incorporate
uncertainty into the derived
means used to calculate
the convex hulls
•They incorporate
information of every part of
the isotopic niche space
•They are affected by
sample size or variability in
the number of groups and
comparisons between
studies, sites or seasons
may be biased
•They can be applied to
compare systems/food
webs only when a small
number of resources is
present
•SEA can be biased with
sample size n< 10 per
group member
•They visualize the
individual level of niche
variation
Standard Ellipse Areas
(SEAs) (Jackson et al.,
2011)
Of a bivariate isotopic (δ13C and
δ15N) dataset , the SEA
represents its true distribution.
The ellipse shape is given by
the dataset associated
covariance matrix whereas its
location is defined by the means
of the bivariate isotopic data
They provide visually straight
forward information on the
degree of trophic variability
at the intrapopulation level
integrating in the measures
the uncertainty and variability
of the data
Cons
•They incorporate each
individual sample
•SEAb : the analysis returns
a posterior distribution of
the metrics providing a
measure of uncertainty and
allowing statistical
comparison (probability
associated with the
differences)
43
Chapter I. General introduction
Table 3 Continued
What
Applicability
Pros
Cons
•SEAc: in case of small
sample size (n < 10 per
group member) the
calculation of the
covariance matrix can be
corrected for small sample
size
•This method is insensitive
to variations in the number
of groups therefore it is
possible to compare
different systems/food
webs/ seasons etc.
• Bayesian-based
approach which integrates
in the measure the
uncertainty and variation of
the dataset
44
Chapter I. General introduction
4.4. Stable isotopes addition to trace carbon fluxes
To understand the possible effects of regime shifts and other climate
change-related effects on Antarctic benthic communities requires a better
understanding of the feeding habits of the organisms of interest and their
role in benthic-pelagic coupling. For the larger organisms (macro- and
megafauna), stable isotope analyses (or other biomarker analyses) can be
combined with in situ observations and gut content analyses to obtain more
detailed insights into the ontogenetic dietary shifts of species and the
trophic relationships between them (Davis et al., 2012). In view of their small
size, the investigation of meiofauna dietary habits represents a difficult task
for ecologists, as direct observation of their feeding behaviour in vivo and
gut content analysis is not easy (if not impossible) to carry out. In this
context enrichment experiments with stable isotopes can represent a
valuable tool. Next to the natural range of stable isotope ratio values for the
various ecosystems and organisms, tracer experiments with sources that
are enriched/labelled in a specific stable isotope provide an extra tool to
gain insight into the interactions among species and trophic pathways (Fry,
2006). Since δ13C is a source indicator, in laboratory experiments it is
possible to enrich a specific medium or food source in the 13C stable
isotope. Once organisms are exposed to this source, the uptake of this
labelled organic matter into the consumer’s body can be tracked, and
“abnormal” variations in their δ13C isotopic signature identified. Values that
differ greatly from the natural background isotopic composition point to an
uptake of the given enriched food and allow estimation of carbon uptake,
providing information on the organism’s role within the ecosystem carbon
flux (Evrard et al., 2010; Fry, 2006; Ingels et al., 2010; Moens et al., 2007).
Many studies have demonstrated the traceability of several 13C-labelled
food sources in meiofauna of various natural marine environments (Carman
and Fry, 2002; Evrard et al., 2010; Ingels et al., 2010a, 2010b; Meyer-Reil et
al., 1980; Nascimento et al., 2008; Pape et al., 2013). However, for Antarctic
meiofauna, only the studies of Moens et al. (2007) and (Ingels et al., 2010a)
has examined the uptake of 13C-labeled carbon sources. Chapter V
examines the possible food preferences of major meiofauna taxa when
provided with detritus of phytoplanktonic or benthic origin, in order to
unravel their role in the overall benthic carbon flux.
5.
Thesis outline
To date there has been very little study of PC meiobenthos and its possible
responses to seasonal food input, or tolerance to inorganic sedimentation or
ice scour disturbance. Investigations of food preferences in light of the likely
45
Chapter I. General introduction
occurrence of regime shifts in the primary producer communities (Moline et
al., 2004; Quartino et al., 2013) are lacking to date. Meio- and macroendobenthos have not yet been investigated in terms of their trophic
interactions and possible responses to local glacial retreat, information
which is essential for understanding possible future benthic community
shifts in response to the ongoing environmental changes. This study set out
to investigate the benthic assemblage structure at three sites with
contrasting
“age-since-retreat”
and
glacier-related
environmental
conditions, and to understand their degree of trophic variability at the intrapopulation level.
The present thesis addresses the following general questions:
i)
Are meiofauna (and endobenthic macrofauna) organisms affected
by locally different glacier retreat-related conditions and do they
respond to these stressors through changes in terms of community
structure and/or trophic interactions?
Are the small sized meiobenthic organisms tuned to the
seasonality in primary production and hence sensitive to possible
changes in the seasonal dynamics?
ii)
This thesis addresses these questions in a two-fold way, focusing on the
shallow water (15 m depth) soft bottom assemblages:


In field studies:
Chapter II - Spatial analysis: three shallo water (15 m ) sites (namely
Faro, Isla D and Creek) were identified in the inner cove in light of
their different “age-since-retreat” and contrasting glacier-retreatrelated disturbances. We sampled inbenthic meiofauna and
macrofauna (and microbiota) in the austral summer 2011 and 2012.
This study investigated the benthic ecology in relation to sediment
biogeochemical characteristics.
Related published work: Pasotti et al., Antarctic shallow water
benthos in an area of recent rapid glacier retreat, Mar. Ecol.,
doi:10.1111/maec.12179, 2014. The first Author was responsible for
the planning of the sampling campaigns, participated to the first of
them where she collected most of the biological and environmental
material. She counted and identified the meiobenthic and
macrobenthic organisms resulting from both the campaigns. She
performed the overall data analysis and lead the writing of the
manuscript.
46
Chapter I. General introduction

Chapter III - Trophic interactions: at the same three study sites and
at same sampling periods (austral summer 2011/2012) the
assemblages’ trophic niches were analysed by means of dual stable
isotope (δ13C and δ15N) techniques along with investigation of
possible functional responses of the assemblage trophic
organisation under specific glacier retreat influences.
Related submitted work: Pasotti, F., et al., Benthic trophic
interactions in an Antarctic shallow water ecosystem affected by
recent glacier retreat, Biogeosciences, 2014. The frist Author

designed and performed the sampling, carried out the processing of
the material, organized the data and contributed in the design,
performance and interpretation of the analysis in R. She lead the
writing of the manuscript.
Chapter IV - Temporal analysis: the meiofaunal and nematode
communities were studied at two contrasting sites (on opposite
shores, one experiencing the melt water plume, the other receiving
particle-free waters from Maxwell Bay, ST1 and ST2) in summer and
winter 2009-2010, and community structure related to sediment
biogeochemical characteristics was investigated.
Related published work: Pasotti, F., Convey, P. and Vanreusel, A.:
Potter Cove (west Antarctic Peninsula) shallow water meiofauna: a
seasonal snapshot, Ant. Sci., 10, 1-10, 2014. The first author
designed and carried out the sampling campaign, the samples
processing as well as the statistical analysis. She lead the writing of
the manuscript.


Experimental studies:
Chapter V - Tracer experiment: the preferred carbon uptake by
major meiofaunal taxa when given pre-labelled (13C) food sources of
different origins (bacteria versus phytoplankton) was investigated
during an experiment carried out in November 2007.
Related published work: Pasotti, F., De Troch, M., Raes, M. and
Vanreusel, A.: Feeding ecology of shallow water meiofauna: insights
from a stable isotope tracer experiment in Potter Cove, King George
Island, Antarctica, Polar Biol., 35(11), 1629–1640, 2012. The first
author processed the samples, carried out the stable isotope
statistical analysis, interpreted the results and lead the manuscript.

Chapter VI - Sedimentation and selectivity experiment: the
responses of meiofaunal organisms to sudden inorganic sediment
load and to variable detritus food sources were investigated, the
latter with the addition of mechanical stress aimed at mimicking ice
47
Chapter I. General introduction
scour disturbance. Sediment was sampled at St7 (or Faro station) in
February 2010.
Related manuscript in preparation: Pasotti F., De Troch, M. and
Vanreusel, A.: “To cope or not to cope?” Can Antarctic meiofauna
cope with impacts from glacier-retreat? Insights from two laboratory
experiments. The first author designed and performed the
experiments, processed the samples, carried out the statistical
analysis and lead the writing of the manuscript.
48
Chapter II. Spatial analysis
The “Three Brothers – Tres Hermanos” hill
“The land looks like a fairytale”
Roald Amudsen
Antarctic explorer
(1872-1928)
Chapter II. Spatial analysis
Adapted from:
Pasotti, F., Manini, E., Giovannelli, D., Wölfl, A.-C., Monien, D., Verleyen, E.,
Braeckman, U., Abele, D. and Vanreusel, A.: Antarctic shallow water
benthos in an area of recent rapid glacier retreat, Mar. Ecol.,
doi:10.1111/maec.12179, 2014.
Abstract
The West Antarctic Peninsula is one of the fastest warming regions on Earth.
Faster glacier retreat and related calving events lead to more frequent
iceberg scouring, fresh water input and higher sediment loads, which in
turn affect shallow water benthic marine assemblages in coastal regions. In
addition, ice retreat creates new benthic substrates for colonization. We
investigated three size classes of benthic biota (microbenthos, meiofauna
and macrofauna) at three sites in Potter Cove (King George Island, West
Antarctic Peninsula) situated at similar water depths but experiencing
different disturbance regimes related to glacier retreat. This study across
different size spectra of the benthos is unique for the Antarctic shallow
water marine environment. Our results revealed the presence of a patchy
distribution of highly divergent benthic assemblages within a relatively small
area (about 1 km2). In areas with frequent ice scouring and higher sediment
accumulation rates, an assemblage mainly dominated by macrobenthic
scavengers (such as the polychaete Barrukia cristata), vagile organisms,
and younger individuals of sessile species (such as the bivalve Yoldia
eightsi) was found. Macrofauna were low in abundance and very patchily
distributed in recently ice-free areas close to the glacier, whereas the
pioneer nematode genus Microlaimus reached a higher relative abundance
in these newly exposed sites. The most diverse and abundant macrofaunal
assemblage was found in areas most remote from recent glacier influence.
By contrast the meiofauna showed relatively low densities in these areas.
The three benthic size classes appeared to respond in different ways to
disturbances likely related to ice retreat, suggesting that the capacity to
adapt and colonize habitats is dependent on both body size and specific
life traits. We predict that, under continued deglaciation, more diverse, but
less patchy, benthic assemblages will become established in areas out of
reach of glacier-related disturbance.
1. Introduction
The West Antarctic Peninsula (WAP) is widely known to be one of the fastest
warming regions on Earth, with an increase in some regions of 1.09°C dec -1
49
Chapter II. Spatial analysis
in winter and a total increase in mean annual air temperatures of around 2.8
°C over the last half century (period 1961-2000) (Turner et al., 2005;
Vaughan et al., 2003). Glaciers along the WAP have been retreating rapidly
since the 1950s (Cook et al., 2005). Glacial retreat impacts the local marine
environment. Large amounts of ice can be released in one single calving
event, potentially leading to abrupt increases in water turbidity, freshening
of surface waters (Dierssen et al., 2002), and the formation of icebergs and
coastal brash ice. In general the impact of icebergs can be detected down
to 600 m depth, and occasionally up to 1000 m, on the Antarctic continental
shelf, where it represents one of the main disturbances, causing the patchy
(fragmented) structure of the benthic communities (Convey et al., 2012 and
references therein ; Gutt, 2001; Smale and Barnes, 2008). In shallow waters
and in the vicinity of the glacier fronts, frequent ice scouring events have a
major structuring effect on benthic communities (Gutt, 2001; Philipp et al.,
2011; Sahade et al., 1998b, 2008; Smale et al., 2008a, 2008b). Glacier
retreat also opens up newly exposed substrata for colonization (Quartino et
al., 2013; Rückamp et al., 2011). In addition to enhanced glacier calving,
regional changes also include enhanced snow melting, which speeds up
ice and permafrost melting and can lead to sudden freshening events and
increased turbidity in the marine coastal environment during warm summer
periods (Dierssen et al., 2002; Hass et al., 2010; Schloss et al., 2002).
The present study investigates the shallow water benthos, associated with
soft sediments in Potter Cove (PC, King George Island, WAP) within the
context of a wider ecosystem study (ESF-PolarClimate, IMCOAST,
www.imcoast.org) which aimed at assessing the complex changes affecting
WAP shallow water environments. Aerial photography and satellite images
document the fast retreat of the Fourcade Glacier since 1956 (Rückamp et
al., 2011). Extrapolations from sediment core data indicate that this glacier
has been retreating during at least the past 100 years, with an acceleration
in the retreat rate since the 1940s (Monien et al., 2011; Rückamp et al.,
2011). This investigation will comprehend three size classes of benthic
organisms: the microbiota (mainly prokaryotes and microphytobenthos),
meiofauna and macrofauna. Studies that cover different size spectra in the
Antarctic are rare (e.g. Peck et al. (1999) investigated effects of iceberg
scour on meio- and macrofauna) and mostly are in the form of reviews on
biodiversity and distribution making use of analysis of historical datasets
(Brandt et al., 2007; Griffiths, 2010). Therefore this study can be considered
unique for the shallow water Antarctic environment.
By comparing the benthic biota and environmental parameters from soft
sediments at three sampling sites in the cove which differ with respect
50
Chapter II. Spatial analysis
duration of ice-free period and impact of the consequences of glacial
retreat, we addressed the following specific questions: (1) Is the structure
and composition of benthic assemblages different between areas under
different glacier retreat impact? (2) do different taxa and size classes differ
in their response to differences in environmental conditions resulting from
glacier retreat?
Fig. 1 Map of Potter Cove showing its location in respect to the Antarctic continent
(top left) and within King George Island (bottom left). The retreat lines of the
Fourcade Glacier are indicated; the three sampling stations are presented in orange.
Background image: SPOT satellite image, 2011-01-15, (c) ESA TPM, 2011.
2.
Material and Methods
2.1. Study sites
Potter Cove is a small fjord-like inlet on the southern coast of King George
Island (South Shetland Islands, Fig. 1). Sandy sediments predominate in
exposed areas of the cove, whereas silt and clay are found in less exposed
locations (Veit-Köhler, 1998). The fine material is mainly deposited in the
deeper basins in the inner cove and close to the glacier front (Wölfl et al.,
2014). The inner part of PC, with a maximum depth of 50 m, is
characterized by a clockwise circulation from Maxwell Bay that enters from
the north and exits in the southern coastal area (Roese and Drabble, 1998;
Schloss et al., 2012). The water that enters carries little suspended
sediment. The south coast of the cove is mostly flat and meltwater streams
carry sediments into the coastal areas during the summer months (Eraso
51
Chapter II. Spatial analysis
and Dominguez, 2007; Schloss et al., 2002). While the major part of this
sedimentary run-off is transported into the adjacent Maxwell Bay (Monien et
al., 2013), sedimentation of this inorganic material also affects the newly
ice-free areas within the cove
We sampled three shallow water stations (each at a depth of 15 m) in the
inner cove, which are influenced by different glacial, meltwater, and water
current conditions. Isla D (62° 13' 32.6" S, 58° 38' 32" W) is the most
recently ice-free area, being exposed since 2003, and situated about 200215 m away from the glacier front. Faro station (62° 13' 32.6" S, 58° 40'
03.7"W) is situated on the northern side of the cove and became ice-free
between 1988 and 1995. It is an area that is characterized by low ice
disturbance and it is affected by wave action (Wölfl et al. in prep.). The third
station, “Creek Station” was located adjacent to “Potter Creek” (62° 13‘
57.3" S, 58° 39’ 25.9" W). This location has been ice-free since the early
1950s and is influenced by a meltwater river that forms during summer. It is
also an area where the impact of growler ice, which can scour the benthos
in PC up to a depth of 20 m (Kowalke and Abele, 1998; Sahade et al.,
1998b) is high.
Benthic samples were collected over two consecutive years each time in
March by scuba divers from the Argentinian/German Carlini (former Jubany)
Station. Samples obtained in 2011 were analysed for meiofauna,
prokaryotes and environmental description. In 2012 further samples were
obtained for macrofauna analysis. Samples for granulometry and organic
content analysis from all study sites were obtained in November and
December 2010.
2.2. Environmental variables
Sediment deposition rate
Clear cylindrical Plexiglas tubes (height (h): 25.3 cm, diameter (d):
4.19 cm, h/d: 6.04) were used as sediment traps. This type is adequate
due to its diameter/ height ratio, which prevents sediment re-suspension
within the tube (Hakånson et al., 1989). In summer 2011 all three locations
were sampled once. In 2012 sediment traps were deployed four times
during January and February (Faro, Creek). On each occasion, two
replicate traps were placed at each study location. The traps were
deployed without fixative for 7 d. The main particle flux in Potter Cove
consists of inorganic material (av. 90%, Khim et al., 2007), and fluxes can
reach up to 130 g m-2 d-1, (Schloss et al., 1999). Occasionally, poor
52
Chapter II. Spatial analysis
weather delayed trap recovery for up to 14 d. Location coordinates,
sampling frames and raw data are available from the PANGAEA database
(doi: 10.1594/PANGAEA.815209). Collected trap material was filtered over
pre-weighted polycarbonate filters (Millipore, Billerica, MA, USA). After
careful washing with 20 mL 18.2 MΩ water, the filters were stored at 4°C,
and subsequently dried at 60°C for 12 h. Data were averaged by stations
and extrapolated to estimate the annual flux (g cm-2 yr-1), considering
glacier activity with sediment discharge of 183 days, based on average
fluvial flow on King George Island (Eraso and Dominguez, 2007). Although
these sediment trap data provide temporal snapshots, they provide recent
sedimentation characteristics for the three investigated locations.
Sediment composition characteristics
Surface sediment samples were taken with a Van Veen grab sampler. One
sample was taken at each study location for measurement of grain size
distribution on a complete sampling grid within a sediment characterization
study in Potter Cove (Wölfl et al., 2014). For each of these stations organic
carbon, carbonate and nitrogen contents were analyzed. Prior to grain size
analysis, acetic acid and hydrogen peroxide were added to the sediment
samples to remove carbonate and organic matter. Samples were mixed
with sodium polyphosphate on an orbital shaker to avoid aggregation of
particles. The analyses were performed using a particle size analyser
(CILAS 1180L, CILAS, Orleans, France), which measures particles between
0.04 and 2500 µm in volume percent. Grain size distributions were
evaluated with the GRADISTAT program (Blott and Pye 2001), and
graphical measures after Folk and Ward (1957) were used for further
applications.
Preparation of total organic carbon (TOC) expressed as %C org, total
nitrogen (TN) samples (expressed as %N) and total carbon (TC) included
drying and homogenization of the sediment. Additionally, the TOC samples
were decarbonated by adding 37% HCl (purity grade). TOC contents were
determined by combustion using an ELTRA CS2000 (ELTRA, Haan,
Germany), TC and TN contents were measured using an Elementar Vario
ELIII, (elementar Analysensysteme, Germany), respectively.
Photosynthetic pigment content
Sediment cores were sliced to obtain 0-1cm, 1-3 cm and 3-5 cm layers. The
analysis of chlorophyll-a (Chl-a) and phaeopigments was carried out
according to Lorenzen and Jeffrey (1980). Pigments were extracted (12 h at
53
Chapter II. Spatial analysis
4 °C in the dark) from each layer using 5 ml of 90% acetone. Extracts were
analysed fluorometrically to estimate the chlorophyll-a and phaeopigment
concentration, the latter after acidification with 200 ml 0.1N HCl. The
concentrations of Chl-a and phaeopigments (expressed in µg/g of dry
sediment) were summed to obtain the total chlorophyll concentration
(Chloroplast Pigments Equivalent, CPE; dataset to be found at
doi.pangaea.de/10.1594/PANGAEA. 815192).
Sedimentary organic matter
Total protein concentration was determined on sediment sub-samples
according to Hartree (1972). Protein concentrations (PRT) were expressed
as bovine serum albumin (BSA) equivalents. Total carbohydrates were
analysed according to Gerchakov and Hatcher (1972) and expressed as
glucose equivalents. Total lipids were extracted from the sediment by direct
elution with chloroform and methanol (1:1 v/v) according to Bligh and Dyer
(1959) and then determined according to Marsh and Weinstein (1966).
Analyses were performed spectrophotometrically. Carbohydrate (CHO),
protein and lipid (LIP) concentrations were converted to carbon equivalents
using the conversion factors 0.40 and 0.49 and 0.75 mg C mg-1,
respectively, and normalised to sediment dry weight (Danovaro et al., 1999;
Fabiano et al., 1995). The ratio between PRT and CHO (PRT/CHO) was
considered as indicative of the aging of the organic matter (Sara et al.,
1999). Biopolymeric organic C (BPC) was calculated as the sum of the C
equivalents of proteins, lipids and carbohydrates (dataset to be found at:
doi.pangaea.de/10.1594/PANGAEA.815193).
2.3. Biota
Prokaryotic abundance and biomass
Three sediment push cores (5.4 cm inner diameter, 22.89 cm2 surface) per
station were obtained in March 2011 and were sliced in 0-1 and 3-5 cm
depth profiles. The intermediate layer 1-3 cm is not reported due to loss
during processing and the consequent lack of a sufficient number of
replicates for the analysis. Nevertheless the surface and deeper layer are
representative enough of the microbial conditions within the sediment
profile analysed. Total prokaryotic number (TPN) was obtained using a
staining technique with Acridine Orange (Luna et al., 2002). Briefly, 0.5 g
sub-samples of each replicate/layer were diluted in tetrasodium
pyrophosphate and incubated for 15 min before sonication. Subsequently
samples were stained with Acridine Orange (final concentration 0.025%),
54
Chapter II. Spatial analysis
filtered over 0.2 µm pore size polycarbonate filters under low vacuum and
analyzed as described by Fry (1990), using epifluorescence microscopy
(1000x magnification). For each filter, between 10 and 20 microscope fields
were counted, corresponding to ca. 400 cells.
Prokaryotic biomass (TPBM) was estimated using epifluorescence
microscopy (Zeiss Axioskop 2, Arese (Milan), Italy, 1000x magnification).
Image analysis was carried out using the ImageJ free software
(http://rsb.info.nih.gov/ij/). Maximum width and length of prokaryotic cells
were measured and converted to bio-volumes, assuming on average C
content of 310 fg C µm-3 (Fry, 1990). TPN and TPBM were normalized to
sediment dry weight after desiccation of a sediment aliquot (24 h at 60 °C).
Datasets to be found at: doi:10.1594/PANGAEA.815194.
Diatom assemblage structure
Diatoms were prepared following Renberg (1990), embedded in Naphrax®
(Brunel Microscopes Ltd, Chippenham, UK) and counted using a Zeiss
axiophot (Carl Zeiss SpA, Arese (Milan), Italy) light microscope with
immersion oil for 100x magnification. Taxonomic identification and
assessment of habitat preferences followed Cremer et al. (2003) and AlHandal
and
Wulff
(2008).
Dataset
to
be
found
at:
doi:10.1594/PANGAEA.815200.
Meiofauna abundance and biomass
At each station at least 3 replicates were obtained on each sampling
occasion. The sediment cores were sliced (0-1, 1-2, 2-5 cm depth) and
stored in formaldehyde (4%, buffered with sea water) until extraction. The
extraction of meiofauna followed standard procedures of centrifugation–
rotation with LUDOX HS40, and sieving over 1,000 and 32 µm sieves (Heip
et al., 1985; Vincx, 1996). Meiofaunal taxa identification and counting
followed Higgins and Thiel (1988).
Nematodes were identified at the genus level. About 60 individuals were
collected randomly from each replicate and each layer of sediment and
mounted on glass slides. The identification keys for free-living marine
nematodes (NeMysKey©) developed within Nemys (http://nemys.ugent.be/)
and by Warwick et al. (1998) were used.
Biomass was estimated for nematodes, copepods, cumaceans and
polychaetes. Biomass (µg C 10 cm-2) of individual nematodes, copepods
and cumaceans was estimated based on the total µg C content of samples
55
Chapter II. Spatial analysis
used for the analysis of the natural δ13C signatures values of these animals
(Pasotti et al., in prep), divided by the number of individuals picked out per
sample. The resulting value was then multiplied by the total number of
individuals (per 10 cm-2) for each layer to obtain biomass estimates per
taxon and layer. The carbon content of the entire samples was determined
using a PDZ Europa ANCA-GSL elemental analyzer 230 (UC Davis Stable
Isotope Facility). For polychaetes, the total number of individuals obtained
was used for stable isotope analysis in order to estimate their biomass in
each layer. All datasets to be found at: doi:10.1594/PANGAEA.815189doi:10.1594/PANGAEA.815190.
Macrofauna abundance and biomass
At each station five replicate samples were taken for macrofauna analysis
with a 16.5*16.5 cm van Veen grab operated from a zodiac. The samples
were washed over a 1 mm mesh, and the total number of individuals sorted
by morphotype and stored in formaldehyde (8% buffered in sea water) until
counting. Deep burrowing species such as the bivalve Laternula elliptica or
ascidians were not counted, since the sampling gear was not appropriate to
evaluate their abundance or biomass. Abundances were expressed as the
total number of individuals per m2 (ind. m-2). Where possible, identification
was made to species level and otherwise to family or higher taxonomic
level. Biomass was estimated as ash free dry weight of the organisms.
Animals were sorted into taxonomic groups, placed into pre-weighed
ceramic cups and dried at 60 °C for 48h. The weight was measured again
after drying in order to obtain the dry weight of the animals, and the
samples were then placed in a muffle furnace at 500°C overnight. The
weight of the remaining ash was subtracted from the dry weight to calculate
the ash free dry weight (AFDW, g m-2). For most taxa, an estimation of the
total biomass was obtained from a subsample of individuals in order to
preserve specimens for other purposes. The bivalve Yoldia eightsi was
divided into size subclasses (big >2 cm; medium 1.5-2 cm; small 1 -1.5 cm,
very small <1 cm) and individuals belonging to each subclass were
removed from the shell and processed for AFDW. Tube-dwelling
polychaetes were processed after removal from the tube. Specimens of
Barrukia cristata (also known as Gattyana cristata) and Aglaophamus
trissophyllus were also divided in size classes according to body length.
Barrukia cristata individuals were weighed after removal of scales, as some
individuals did not possess a complete set of scales when sampled.
Similarly, for the serolid isopod Paraserolis polita and the pennatulid
Malacobelemnon daytoni, length size classes were used. All datasets to be
found at: doi:10.1594/PANGAEA.815187- doi:10.1594/PANGAEA.815188.
56
Chapter II. Spatial analysis
Trophic composition
The trophic diversity of the nematode assemblage was determined within
the upper 0–5 cm of sediment, using the classification system of Wieser
(1953). The trophic guilds that characterize the nematode assemblage are:
selective deposit feeders (1A), characterized by a small buccal cavity and
assumed to feed selectively on bacteria; non selective-deposit feeders (1B)
showing a larger unarmed buccal cavity and expected to feed by injestion
on detritus and sediment particulate organic matter; epistrate feeders (2A),
which usually feed (by piercing through their shells) on microalgae or other
small unicellular organisms and have buccal cavities with one or more small
teeth; predators/omnivores (2B), which are normally larger nematodes with
large teeth and/or mandibles, and predate on other meiofauna organisms
and/or ingest detritus particles.
Macrofauna were merged in trophic feeding groups based on the literature
and stable isotope analysis (Corbisier et al., 2004; Macdonald et al., 2010;
Siciński et al., 2011); Pasotti et al., unpubl. data). The trophic groups are:
predators (Pr) (including scavengers); Omnivores (Om); deposit feeders
(De), which feed on deposited organic matter including microalgae and
bacteria; deposit and/or suspension feeders (De/Su) which can switch
between feeding on deposited organic matter or filter particulate organic
matter in suspension in the water column; filter feeders (Ff) which feed
selectively on particles suspended in the water column; and grazers (Gr),
which strictly feed on micro- or macroalgae.
2.4. Statistical analysis
To test for differences in vertical profiles of meiofaunal density/biomass,
prokaryotic density/biomass, and environmental variables (combined and
individually), non-parametric permutational ANOVAs (Permanova) with a
fully crossed three-factor design were performed with random factor
replicate “re” nested in the fixed factor station “st”, next to the fixed factor
layer “la”. With this design we resolve the problem of ”non independence of
data” from contiguous layers parameter’s values (e.g. nematode
abundances in the first layer are linked to abundances in the second layer
etc.. when considering the complete depth profiles abundance), shuffling
the same layers between the replicates of each station (we nested random
factor “re” in fixed factor “st”).The interaction term “st×la” informs about the
difference in depth profiles of environmental parameters between the
57
Chapter II. Spatial analysis
stations. This type of analysis is equivalent to use of univariate ANOVAs with
p-values obtained by permutation (Anderson and Millar, 2004) and is
therefore more robust against violation of normality. An Euclidean distance
based resemblance matrix was used for the analysis of the environmental
variables, and a Bray Curtis similarity resemblance matrix was used for the
abundance and biomass data. In case of significant “st×la” interactions,
pair wise tests of “st” and “la” within “st×la” were performed to determine
which of the layers differed significantly between stations. Because of the
restricted number of possible permutations in pairwise tests, p-values were
obtained from Monte Carlo samplings (Anderson and Robinson, 2003).
Permdisp confirmed homogeneity of multivariate dispersion for any of the
tested terms in each Permanova. Since the assemblages were sampled in
bulk (via van Veen grab), we performed one-way non-parametric
permutational ANOVAs (one-way Permanovas) for macrofauna densities,
biomasses and trophic structure, in which a single fixed factor station “st”
was considered during the analysis. If the factor “st” was significant, a
pairwise test was performed. Again, in the light of the restricted number of
possible permutations in the pairwise tests, p-values were obtained from
Monte Carlo samplings (Anderson & Robinson 2003). Similarity percentage
analysis (SIMPER) was performed on the (bulk, no layer difference taken
into account) nematode genera and macrofaunal datasets, in order to
identify the most important taxa contributing to the differences in biomass
and abundance between the stations. Non-metric Multi Dimensional Scaling
(nMDS) was performed on meiofauna and macrofauna abundances in order
to better visualize the data. Abundance and biomass data were fourth root
transformed prior to each analysis in order to downweight the influence of
the more abundant taxa (e.g. nematodes). Environmental data were
normalized when variables with different unit measures were analyzed
together. For the sediment trap material, insufficient data were available to
perform statistical analysis. We therefore provide the data as a box plot, to
display the full variability. The results are reported as mean values ±
standard deviation.
58
Chapter II. Spatial analysis
3.
Results
Table 1 summarizes all Permanova results and pairwise comparisons
between the three sampling locations.
3.1. Environmental variables
Sediment deposition rate
Sediment deposition rate at the three locations showed high variability (Fig.
2). Faro station had the lowest deposition rate (median 0.12 g cm-2 yr-1,
range 0.06 to 0.18 g cm-2 yr-1). The rate at Creek station was higher
(median 0.45 g cm-2 yr-1, range 0.3 to 0.95 g cm-2 yr-1). The highest rate
was measured at Isla D (1.17 g cm-2 yr-1), but this was based on a single
sediment trap deployment.
Sediment composition characteristics
Sediment composition at the three locations was clearly different (Table 2).
Site specific grain size composition ranged from sand (Creek) to mud (Isla
D) dominated. Faro station displayed a higher percentage of organic
carbon (%Corg), carbonate (% carbonate), as a higher C:N ratio, as well as
Corg/N ratio compared with the two other stations.
Pigments
The concentrations of phaeopigments were two orders of magnitude higher
than the chlorophyll-a concentrations at all three locations (Fig. 3 a and b).
Chl-a and phaeopigment concentrations in the 0-1 cm layer were
significantly higher at Faro and Creek compared to Isla D. Instead Isla D
had a subsurface (1-3 cm) peak in pigment concentration. The pigment
concentrations in the deeper layer (3-5 cm) were higher at Creek than at the
other two locations.
Organic matter composition
At all three locations, proteins were the dominant class of biochemical
organic matter (mean 57.9%), followed by lipids (mean, 31.5%) and
carbohydrates (mean 10.6%) (Fig. 4 a and b). The three classes showed
variable vertical distribution, with significantly lower mean PRT values at Isla
D compared to Faro and Creek. The CHO concentration was comparable in
the upper layer at all three locations whilst, in the 1-3 cm layer, Faro had the
highest CHO concentration, followed by Isla D and Creek. In the deeper
59
Chapter II. Spatial analysis
layer (3-5 cm), Faro showed the highest concentration followed by Creek
and Isla D, with the only significant difference being between Isla D and the
other two stations. The PRT/CHO ratio in the surface layer of Creek was
significantly higher than at Isla D. The 1-3 cm layer of Creek had the highest
PRT/CHO values (though also the highest standard deviation), followed by
Isla D and Faro. In the deeper layer the ratios were similar at all the stations.
PERMANOVA further indicated highly significant differences of the “st×la”
factor (see Table 1) for LIP and BPC between stations but, due to a
significant Permdisp value (distance among centroids grouping factor
“st×la”, Permdisp factor “st”), we do not consider these as representative of
real differences between stations and layers, but rather the result of natural
variability. Creek had higher levels of BPC and lipids than the other two
stations.
Fig. 2 Sediment accumulation rates (g cm-2 yr-1) are given as median, quartiles (box)
and 95% confidence intervals (whiskers) for the different sites Faro, Isla D and Creek.
Please note, site Isla D was sampled only once.
Fig. 3 Chlorophyll-a (a) and phaeopigment (b) concentrations expressed as µg g-1
dry weight per sediment layer (mean ± SD).
60
Chapter II. Spatial analysis
Fig. 4 a) Protein (PRT, blue bars), carbohydrate (CHO, dark red bars) and lipid (LIP,
orange bars) concentrations (mg g-1, left vertical axis) and PRT:CHO ratio (black
rhombus, right vertical axis) in each layer (0-1 cm, 1-3 cm and 3-5 cm) of each
station (mean ± SD). b) Biopolymeric carbon (BPC, mg g-1) and relative contribution
of PRT CHO and LIP (expressed in carbon equivalents) in the 3 stations on a bulk
sediment 0-5 cm profile (mean ± SD).
3.2. Biota
Prokaryotic abundance and biomass
Prokaryotic abundance and biomass were significantly higher in
surface sediments (0-1 cm) from Isla D compared to both Faro and
Creek (Fig. 5). In contrast, the deeper layer (3-5 cm) of sediment at
Faro contained significantly lower numbers of prokaryotes and
related biomass compared to the other two stations.
Diatom assemblage structure
The diatom assemblages were dominated by benthic species at
Faro, whereas taxa associated with sea-ice or normally living in
open waters were more abundant at Creek and particularly at Isla D
(Table 2). Diatom abundance was conspicuously low at Isla D.
Meiofauna abundance and biomass
The total abundance and overall taxonomic composition of the
meiofauna are illustrated in Fig. 6 a and b (see also Addendum
Table_A1). Nematodes were always the most abundant taxon, contributing
93.7% at Faro, 94.5% at Isla D, and 98.1% at Creek. Harpacticoid copepod
abundance and nauplii densities were higher at Isla D. Polychaetes were
the second most abundant taxon at Faro (3.28%), whilst at Creek and Isla D
they contributed 0.51% and 1.08%, respectively.
61
Chapter II. Spatial analysis
Cumaceans reached the highest abundance at Faro (0.4%). The upper
layer (0-1 cm) contained 52% of the total 0-5 cm assemblage at Isla D, and
42% at Faro. At Creek almost half of the assemblage (43%) was
concentrated in the subsurface layer (1-2 cm). Total meiofauna abundance
differed between Isla D and Faro across all three depth layers (see Table
2).
Nematode biomass (Fig. 6 b, Addendum Table A1) did not differ
significantly between stations. Cumacean biomass was highest at Creek,
whereas copepod biomass was significantly higher at Isla D compared to
Faro and Creek.
The nMDS of the meiofauna vertical distribution (Fig 7a) revealed a
relatively higher patchiness at the Isla D and Creek sites compared to Faro.
At the latter station, each replicate layer clustered more closely together in
the two dimensional space compared with the same layers at the other two
sites.
Nematode genus composition and trophic diversity
Nematode assemblage composition on the genus level and trophic diversity
are shown in Fig. 8 a and b, respectively. In general, we found significant
differences in nematode genus composition based on relative abundances
between Isla D and the other two stations in the first layer of sediment (0-1
cm), between all the stations in the subsurface layer (1-2 cm), and between
Isla D and the other two stations in the deeper layer (2-5 cm; Table 2). The
SIMPER analysis of the nematode assemblage showed that Faro was
dominated by Daptonema (40%) and Sabatieria (20%), which are both nonselective deposit feeders (1B). Creek was characterized by a more even
nematode assemblage with Daptonema still being the most abundant taxon
(20%) followed by Aponema (12%) and Acantholaimus (10%). These last
two genera are epistrate feeders (2A). The nematode assemblage at Isla D
was dominated by Daptonema (29%) and Microlaimus (27%); the latter
belongs to the trophic guild 2A.
The three stations showed significant differences in trophic guild
composition. Faro was strongly dominated (76%) by non-selective deposit
feeders (1B), 53% of Isla D nematode assemblage belonged to the
epistrate feeder 2A group, whilst Creek showed a more even nematode
assemblage composed of non-selective deposit feeders (46%) and
epistrate feeders (39%).
62
Chapter II. Spatial analysis
Fig. 5 Prokaryotic abundances (Total Prokaryotic Number, TPN, n° of cells per gram
of sediment) and biomass (Total Prokaryotic BioMass, TPBM, µg C g -1 of sediment)
for the surface (0-1 cm) and deeper (3-5 cm) layers of the three stations. (mean ±
SD).
Table 2 Biogeochemistry and diatoms relative abundance.
Faro
Isla D
% GRAVEL
0.0
0.0
% SAND
63.5
0.9
% MUD
36.5
99.1
% Corg
0.212
0.119
% Carbonate
5.799
2.899
%N
0.042
0.032
C/N
142.044
95.515
Corg/N
5.002
3.771
Diatoms
planktonic/sea ice
benthic
unknown/both
%
12.87129
86.63366
0.49505
%
44.35484
54.83871
0.806452
Creek
0.8
95.7
3.4
0.150
2.662
0.039
72.013
3.833
%
22.94118
40.58824
36.47059
63
Chapter II. Spatial analysis
Table 1 Resumé of permutational ANOVA (PERMANOVA).
'st x la'
'st'
0-1 cm
1-2 cm
2-5 cm
F
F
C
F
F
C
F
F
C
F
F
C
vs
vs
vs
vs
vs
vs
vs
vs
vs
vs
vs
v
s
I
I
C
I
I
C
I
*
ns
ns
*
ns
n
s
< **
< **
ns
<*
<*
ns
n
s
<*
<
***
<*
<*
ns
ns
ns
ns
ns
> **
>*
n
s
*
*
*
*
*
ns
*
'st'
'st x la'
I
C
I
I
C
*
*
*
*
ns
*
ns
Nematodes
ns
ns
Copepods
**
**
*
< **
ns
Meiofauna
Abundances (n° ind. 10 cm-2)
Multivariate
Nauplii
Polychaetes
Cumaceans
***
**
*
*
ns
ns
**
NA
*
*
*
*
*
*
ns
< **
ns
>*
Biomass
µg C 10 cm-2
tot biomass
Nematodes
Copepods
Cumaceans
Nematode TG
Nematode Genus (Rel. Ab.)
**
ns
**
***
***
***
*
< **
ns
<*
> ***
ns
> ***
**
**
ns
***
***
***
> ***
> ***
ns
*
ns
Macrofauna
Abundances (n° ind. m-2)
Total Abundance
Multivariate
Yoldia eightsi
Cirratulidae
Barrukia cristata
Priapulus sp.
Eudorella sp.
Malacobelemnon daytoni
***
**
***
**
*
***
**
***
**
**
***
> ***
ns
> **
<*
>*
<*
ns
**
ns
> ***
> ***
ns
> ***
>*
>*
> ***
> ***
ns
64
Chapter II. Spatial analysis
Table 1
Continued
'st x la'
'st'
'st'
'st x
la'
0-1 cm
1-2 cm
2-5 cm
F
F
C
F
F
C
F
F
C
F
F
C
vs
vs
vs
vs
vs
vs
vs
vs
vs
vs
vs
vs
I
C
I
I
C
I
I
C
I
I
C
I
> **
>*
ns
***
***
**
>
***
> **
>
**
ns
> **
<*
> **
ns
ns
ns
< **
ns
<*
ns
<*
>*
>*
>
***
ns
***
**
Biomass (g
AFDW m-2)
Total biomass
Multivariate
Yoldia eightsi
Cirratulidae
Maldanidae
Barrukia cristata
Aglaophamus
trissophyllus
*
***
***
**
*
*
*
Malacobelemnon
daytoni
***
>
***
>
***
Trophic structure
***
***
Eudorella sp.
**
Prokaryotes
TPN (n° cells g1)b
TPBM (µg C g1)b
Environmental
Chla
Phaopigments
CPE
***
*
<*
ns
<*
NA
NA
NA
< **
<*
ns
***
*
<*
ns
<*
NA
NA
NA
< **
<*
ns
*
***
>*
ns
>*
<*
ns
<
**
< **
<
***
>
*
**
**
**
**
> **
> **
ns
ns
>*
>*
ns
ns
ns
ns
ns
ns
ns
ns
< **
<*
ns
ns
***
***
***
***
***
*
**
**
ns
**
ns
**
ns
*
**
ns
>
**
<*
>*
ns
>
*
***
> **
ns
>
***
>*
***
ns
<
***
>*
ns
ns
>*
> **
ns
Food quality
(PRT,CHO,LIP)a
PRT
CHO
LIPa
> **
ns
>*
PRT/CHO
*
***
ns
ns
>*
<*
<* >*
ns
ns
ns
>
<
>
>
>
***
***
***
***
***
***
ns
>*
***
ns
ns
The signs “>” and “<” are relative to the comparative label (e.g. F vs. I). Significance values are reported as * for
p<0.05, ** for p<0.01 and *** for p<0.0001. When Permdisp analysis gave values p>0.05, no remarks were made.
On the other hand, in case of p<0.05, a was added beside the investigated parameter whereas when the
Permdisp was not possible because of a too low number of levels, b was placed next to the investigated
parameter.
BPCa
65
Chapter II. Spatial analysis
Fig. 6 a) Meiofauna total abundances (mean n° individuals per 10 cm-2 ± SD) with
average layer contribution. b) Meiofauna biomass (mean ± SD): taxa included are
nematodes (more than 90% of biomass in each station), cumaceans and copepods.
c) Abundances of meiofauna taxa with the exclusion of nematodes for the 0-5 cm
profile (average n° individuals per 10 cm-2 ± SD). The “Others” class includes a total
of 19 taxa among which amphipods, priapulids, ostracods and turbellarians.
Macrofauna abundance and biomass
Macrofauna abundances and biomass are summarized in Fig. 9 a,b (values
reported in Table A2 and A3 of the Addendum and SIMPER results are
reported in Table 3 a,b). Macrofauna densities differed significantly
between all three stations (Table 2). In general, the highest total abundance
was found at Faro followed by Isla D and Creek (Fig. 9a). Differences were
also significant for the major taxa between all stations. The nMDS (Fig. 7b)
based on abundances was more scattered in samples from Isla D and
Creek compared to samples from Faro. The latter formed a well-defined
group. Malacobelemnon daytoni (Cnidaria, Pennatulacea) and Priapulus sp.
(Priapulida) were only found at Faro, whilst Barrukia cristata (Polychaeta,
Polynoidae) was only present at Isla D.
Bivalves were more abundant at Creek, where Mysella charcoti (Bivalvia,
Galeommatidae), Genaxinius sp. (Bivalvia, Thyasiridae) and Yoldia eightsi
66
Chapter II. Spatial analysis
(Bivalvia, Nuculanidae) made up about 41.8% of the whole assemblage.
Yoldia eightsi was also present at Faro but at a low relative abundance
(0.68%) and was absent at Isla D. Polychaetes were also abundant, with
little differences in relative abundance between the stations, namely 23% of
the total assemblage at Creek, 27% at Isla D and 28% at Faro. Cirratulidae
(Polychaeta) were the most abundant family found in higher numbers at
Faro, followed by Isla D and Creek. Maldanidae (Polychaeta) were also
present only at Faro. The peracarid crustaceans were mainly represented
by the cumaceans even though the tanaidaceans were also present in very
low numbers at Faro. Cumaceans made up more than 50% of total
abundance at both Faro and Isla D, and only 14% at Creek. The cumacean
macrofauna assemblage at Isla D was composed of three different genera
(Eudorella sp., Diastylis sp. and Vaunthompsonia sp.), whilst only Eudorella
sp. was found at the other two stations. The abundance of amphipods was
only significantly different between Faro and Creek, with Creek being
characterized by the highest density of these crustaceans (Table 7
supplementary material).
Total macrofauna biomass was significantly higher at Faro compared with
both Creek and Isla D (Table 6 supplementary material). The SIMPER
analysis revealed differences in the biomass of larger organisms between
stations (Table 3 b). The assemblage at Faro was composed of Y. eightsi
(56.6% of the total biomass), Paraserolis polita (12.8%) (Crustacea,
Serolidae) Malacobelemnon daytoni (8.9%), and also by Eudorella sp.
(9.4%). The biomass at Creek was dominated by the polynoidae Barrukia
cristata (89% of the total biomass). The biomass at Isla D was more evenly
divided between B. cristata (40% of the total biomass) and Aglaophamus
trissophyllus (22%) (Polychaeta, Nephtydae); Eudorella sp. was scant (6%
of the total biomass).
Macrofauna trophic structure
The trophic diversity based on biomass data was significantly different
between the three stations (see Fig. 10 and Table 4). Three different
assemblages could be defined. At Faro the assemblage was characterized
by a high biomass and composed of deposit/suspension feeders (59%),
omnivores (18%), deposivores (15%), filter feeders (8%) and predators
(0.28%). At Isla D biomass was low, and the assemblage (63%) was
dominated by predators/ scavengers followed by deposit feeders (22%)
and omnivores (13%). At Creek, an assemblage with an intermediate
biomass
was
present,
which
was
dominated
(90%)
by
predators/scavengers.
67
Chapter II. Spatial analysis
Fig. 7 Multi Dimensional Scaling (MDS) based on (above) meiofauna abundances (3
to 4 replicates per site) with the 1= 0-1 cm depth, 2=1-2 cm depth and 3=2-5 cm
depth profiles and (under) macrofauna abundances with the five replicate samples
for each of the sites. The more scattered labels of Creek and Isla D compared to
Faro site may point at a higher patchiness possibly related to disturbance due to the
glacier and creek discharge.
68
Chapter II. Spatial analysis
Table 3 Similarity percentages analysis (SIMPER) results based on (a) nematode genera, (b) macrofauna abundances and (c)
biomasses
(a) Nematode genera
Groups Faro & Isla D
Average dissimilarity = 70,66%
Daptonema
Microlaimus
Sabatieria
Dichromadora
(b) Macrofauna abundances
Groups Creek & Isla D
Average dissimilarity = 66,16%
Eudorella sp.
Yoldia eightsi
Cirratulidae
Mysella charcoti
Dyastilis sp.
Barrukia cristata
(c) Macrofauna biomass
Groups Creek & Isla D
Average dissimilarity = 83,35%
Barrukia cristata
Aglaophamus trissophyllus
Terebellidae
Mysella charcoti
Contrib%
Groups Faro & Creek
Average dissimilarity = 65,96%
Daptonema
Sabatieria
13.26 Aponema
10.2 Linhomoeus
20.75
14.86
Contrib%
11.98
10.03
9.89
9.35
8.96
Groups Creek & Faro
Average dissimilarity = 58,72%
Eudorella sp.
Cirratulidae
Malacobelemnon daytoni
Mysella charcoti
Barrukia cristata
6.7 Priapulus sp.
Contrib%
Groups Creek & Faro
Average dissimilarity = 94,73%
Barrukia cristata
Yoldia eightsi
Paraserolis polita
4.96 Malacobelemnon daytoni
63.65
12.42
5.86
Contrib%
Groups Isla D & Creek
Average dissimilarity = 67,26%
Microlaimus
Daptonema
8.25 Dichromadora
7.98 Aponema
24.33
15.6
Contrib%
18.17
13.96
10.08
8.41
7.28
6.79
Contrib%
Groups Isla D & Faro
Average dissimilarity = 54,57%
Malacobelemnon daytoni
Dyastilis sp.
Eudorella sp.
Yoldia eightsi
14.62
14.09
9.71
8.45
Contrib%
Maldanidae
10.81
8.7
8.29
8.15
7.28
Priapulus sp.
7.28
Groups Isla D & Faro
Average dissimilarity = 92,51%
Yoldia eightsi
Paraserolis polita
Malacobelemnon daytoni
6.28 Eudorella sp.
35.61
35.42
7.33
Contrib%
Contrib%
48.41
9.72
8.64
7.84
69
Chapter II. Spatial analysis
Fig. 8 a) Nematode genus composition of the
0-5 cm profile. The most important genera are
presented with their latin names whilst the other
genera are pulled together in “Others” and
their number is reported. b) Nematode
community trophic diversity of the 0-5 cm
profile based on abundances. 1A= selective
deposit feeders; 1B = non selective deposit
feeders; 2A = epistrate feeders; 2B =
predators/omnivours.
Fig. 9 a) Macrofauna abundances (average n°
individuals ± SD) of the main taxonomic
groups. Bivalves include Yoldia eightsi, Mysella
sp. and Genaxinius sp.;Cumaceans include
Eudorella sp. for three stations and
Dyastilopsis sp and Vauthomsia sp. only for
Isla D; Polychaetes include the families:
Cirratulidae,
Orbinidae,
Terebellidae,
Capitellidae,
Ophaelidae,
Maldanidae,
Spionidae, Polynoidae and Nepthydae. b)
Macrofauna biomass expressed in grams of
ash free dry weight per meter square (g AFDW
m-2 ± SD) with the contribution of the most
important species at the three stations.
Fig. 10 (Left) macrofauna trophic structure
based on biomass. Su= suspension feeders;
Pr= predators; Gr= grazers; Om= Omnivours;
Ff= filter feeders; De= Deposit feeders.
70
Chapter II. Spatial analysis
4.
Discussion
Coastal ecosystems in the Western Antarctic Peninsula have experienced
glacial advance and retreat during the Holocene. The rapid retreat of the
Fourcade tidewater glacier on King George Island during the last 100 years
can, however, be considered as an extreme event which was driven by the
regional climate warming in the WAP (Monien et al., 2011). A trough is
present in the middle of the cove and it now accumulates erosive
sediments, while iceberg scouring led to ice furrows visible in sonar images
of Potter Cove (PC). These features are mainly detected in deeper waters,
most likely due to better preservation than in nearshore and shallower areas
(Wölfl et al., 2014). The dynamics related to glacier retreat in combination
with the oceanographic characteristics (e.g. bathymetry, waves and
currents) of the cove have resulted in a gradual maturation of the
ecosystems away from the glacier front and to the patchy structure in the
benthic assemblages present at the different sites under study. Recently
emerged ice-free areas, such as Faro or Isla D, are subject to colonization
and biological succession by macroalgae and organisms directly
depending on them. The spreading of macroalgal beds on the newly icefree areas in Potter Cove, and their decay and decomposition enhance the
transport of material (both organic carbon and nutrients ) and thus available
energy in deeper benthic habitats (Quartino et al., 2013; Quartino & Boraso
de Zaixso, 2008 and references therein). Here we highlight the possible
drivers for each benthic assemblage identified at the three sites, including
the environmental parameters measured and the possible interactions
between the different biotic and abiotic components, in order to place these
into a context of recent glacial change events.
4.1. Faro
The Faro site became ice-free between 1988 and 1995 (Rückamp et al.,
2011) and ice growler action is thought to be absent (Philipp et al., 2011).
Instead bottom communities at this station are affected by high bed shear
stress and wave action (Wölfl et al., 2014). The large grain sizes found at
Faro indicate that this site does not experience high deposition and fine
sediments are eroded as seen in the analysis of the sediment trap data.
Recently, macroalgae have colonized the hard substrates of this newly icefree area (Quartino et al., 2013). We found higher macrofaunal biomass and
a more homogeneous assemblage compared with the other two stations.
Large mobile predators, such as Nepthydae or Polynoidae polychaetes,
were absent at the time of sampling. The presence of the brooder P. polita
and the high abundances of small polychaetes are usually indicative of low
71
Chapter II. Spatial analysis
ice disturbance and relatively clear waters (Kowalke & Abele, 1998; Smale,
2008). This is corroborated by the dominance of benthic diatom taxa over
planktonic and sea-ice species in the sediment biofilm. The influence of
previous glacial related disturbances on these communities is reflected by
the presence of pennatulids and larger individuals of the bivalve Yoldia
eightsi. These organisms are of low motility but have pelagic larvae with
high dispersal capacities, and are known to be able to rapidly colonize
previously disturbed areas of the Antarctic seabed (Smale, 2008). Yoldia
eightsi is typically found in glacial coves and is potentially capable of
outcompeting the larger Laternula elliptica when the latter is present at low
abundance (Siciński et al., 2012). At Faro only large Y. eightsi of shell width
> 1.5 cm were found. Under iceberg impact smaller and younger
individuals are abundant (Brown et al., 2004). In spite of being inferior
competitors, pennatulids exhibit high growth rates and are often found in
high abundance on bare substrata after physical disturbance, reflecting
their high colonization capacity (Momo et al., 2008; Sahade et al., 1998b).
The dominance of particular suspension and filter-feeders in combination
with subdominant deposit feeders points at frequent re-suspension events,
which support an environment for a specific macrobenthic assemblage,
feeding at the sediment-water interface.
Table 4 Macrofauna feeding groups.
species/taxon
Feeding
group
species/taxon
Feeding
group
Ophaelidae
De
Gasteropoda
Gr
Spionidae
De
Mysella charcoti (Lamy, 1906)
Malacobelemnon daytoni (Lòpez González
Ff
Orbinidae
De
et al., 2009)
Ff
Terebellidae
De
Yoldia eightsi
De / Su
Eudorella sp.
De
Barrukia cristata (Willey, 1902)
Pr
Dyastilopsis sp.
De
Polynoidae
Pr
Vauthompsia sp.
De
Aglaophamus trissophyllus (Grube, 1887)
Pr
Pseudotanais sp.
De
Priapulus sp.
Pr
Maldanidae
Om
Paraserolis polita (Pfeffer, 1987)
Pr
Cirratulidae
Om
Oligochaetes
Om
Amphipodes
Om
Tanaidacea
De= deposit feeder; Om= comprises omnivours which behaves like scavengers, detritus feeders,
grazers non stricto sensu; Gr= grazers stricto sensu; Ff= filter feeders intending organisms
feeding selectively on certain component of the particulate organic matter in the water column;
Su= suspension feeders feeding on suspended particulate matter unselectively; Pr= predators
and scavengers supposed to occupy the higher level of the food web.
72
Chapter II. Spatial analysis
In contrast, both the meiofaunal and the prokaryote assemblages were
characterized by the lowest biomass among the three stations. This is
surprising, given the higher food availability (Chl-a and high BPC)
compared with the other sites. Unsurprisingly for soft sediments, the
meiofaunal assemblage was dominated by nematodes. Polychaetes and
cumaceans were also present, but harpacticoid copepods and their larvae
were virtually absent. A dominance of nematodes and meiobenthic
polychaetes with a lower abundance/frequency of other common taxa (e.g.
harpacticoids and nauplii) was also found in the inner part of Hornsund
Fjord in the High Arctic, a location similarly impacted by rapid glacial retreat
(Grzelak & Kotwicki, 2012), whereas cumaceans were absent. The
nematode assemblage at Faro station was dominated by two genera of
non-selective deposit feeders (Sabatieria in the deeper layers and
Daptonema in the surface layer), which thrive in low oxygen, organically
enriched environments worldwide (Moreno et al., 2008; Soetaert and Heip,
1995; Steyaert, 2003). Daptonema is opportunistic and easily switches
between different food sources such as microalgae and bacteria (Pasotti et
al., 2012; Vanhove et al., 2000). These findings point to a detritus-based
assemblage, which is often associated with hypoxic bottom conditions.
Macroalgal debris is accumulating in this part of the cove and may cause
anoxia in the sediments, explaining lower endobenthic densities and
dominance of Sabatieria and Daptonema (Wetzel et al., 2002). The low
copepod abundance might also relate to the low oxygen concentrations in
the surface layer (Coull, 1970; Giere, 2009).
4.2. Isla D
The upper sediment layers at this location were muddy and soft, and the
sediment accumulation rates relatively high compared to the other two
stations. BPC was the lowest compared with the other stations and the
organic matter in the surface layer appeared to be old (high CHO%, low
BPC, low PRT/CHO) (Pusceddu et al., 1999). Low organic carbon content,
BPC, diatom and Chl-a concentrations at Isla D are likely to be a
consequence of the local high sedimentation of inorganic sub-glacial
derived material. Moreover, the low primary production is probably related
to the typically high turbidity and low light conditions, caused by the
combination of brash ice movements and glacial discharge. Isla D is
located in an area of the inner cove where wave action is negligible and
therefore stands for a low energy environment, which is also reflected in the
occurrence of fine sediments.
73
Chapter II. Spatial analysis
The macrofaunal assemblage at Isla D was relatively poor in terms of both
density and biomass when compared to the other two sites. It also showed
a highly patchy distribution revealed in the nMDS analysis. It is likely that
the assemblage at this site represents a recent colonization stage in a high
sedimentation
(low
energy)/glacier
calving-related
disturbance
environment. This is confirmed by the dominance of cumaceans and
relatively large polychaete species such as the vagile predator
Aglaophamus trissophyllus and the motile scavenger Barrukia cristata.
Cumaceans are successful organisms in areas with high sediment
accumulation rates, whereas small infaunal polychaetes typically arrive at a
later successional stage when physical disturbance is lower (Kowalke &
Abele, 1998). Vagile secondary consumers are generally indicative of
locations affected by ice disturbance (Smale 2007; Smale, 2008; Siciński et
al., 2012). Devastating as it is for many sessile species, ice-scouring events
also produce dead animal material for scavengers such as B. cristata.
Compared to Faro, filter and suspension feeders were lacking at Isla D. This
may be due to the presence of high sediment loads in the waters which can
exert a negative effect on filter-feeding activity, through dilution or clogging
of the filter apparatus.
Contrasting with the macrofauna, prokaryotic biomass and abundance at
Isla D were the highest of all three stations. The meiofauna showed the
highest number of individuals, and, only at Isla D, copepods and nauplii
were relatively abundant, in spite of their general preference for coarser
sediments (Vanhove et al., 2000; Pasotti et al., 2012). This might be
counteracted by their ability to colonize barren substrates such as sites
after iceberg scouring (Lee et al., 2001b; Veit-Köhler et al., 2008b). The
presence of copepods and a richer meiofaunal assemblage indicates
relatively well-oxygenated conditions. The nematode assemblage was
dominated by epistrate feeders (50%, e.g. Dichromadora and Microlaimus)
followed by non-selective deposit feeders. The high proportion of nonselective deposit-feeding nematodes possibly reflects the important role of
the benthic microbial assemblage in their diet (Wieser, 1953) and indicates
that they play an important role in the benthic food web. The latter is
truncated towards smaller organisms, as evidenced by the relatively high
number and biomass of prokaryotes and dominance of meiofauna over
macrofauna. The lower transfer of organic matter to the macrofauna level
suggests that this system may act as a carbon sink. The subsurface Chl-a
peak may support the high abundance of epistrate feeders such as
Dichromadora in the deeper layers, and the higher abundance of
prokaryotes in the surface layer may be the cause of the dominance of
Daptonema. Furthermore the second dominant genus, Microlaimus, is
74
Chapter II. Spatial analysis
known to be a relatively rapid colonizer (Wetzel et al., 2002) and has been
reported as the dominant taxon after iceberg scouring (Lee et al., 2001b).
These observations are consistent with a hypothesis that the sediments at
Isla D are at an early stage of meiofaunal colonization, during which the
organisms benefit from the less disturbed sedimentary conditions and need
to be tolerant of high sediment deposition rates. Nonetheless the nMDS of
meiofauna for this site shows a relatively more scattered distribution of the
replicate layers compared to Faro, highlighting a higher micropatchiness at
this site.
4.3. Creek
Of the three stations, Creek has the longest ice-free history of more than 50
years. The creek flows during the summer months and is fed by glacierand snowmelt as well as by groundwater drainage through moraines (Eraso
and Dominguez, 2007; Varela, 1998). The location experiences the
discharge of highly suspended particle laden melt water, although our
measured sediment accumulation rates are lower than the values estimated
from the single sediment trap deployment at Isla D. High melt water
discharge can also result in sediment re-suspension, in spite of usually low
bed shear stress recorded at this site (Wölfl et al., 2014). The riverine
meltwater transports large quantities of coarse and fine material from the
land to the beach. Here waves and tides brings the material into the sea.
The depositional material is carried away from the source on the base of its
size fraction, with coarses (heavier) material being deposited in the vicinity
of the river source, whereas the finer component can be transported much
further away (depending on current intensity). This may justify the low
organic content observed at this staton. In fact, the generally clock-wise
wind-driven current pattern in Potter Cove (Klöser et al., 1994; Roese and
Drabble, 1998) exports sediment laden waters - and likely the organic
particles adehered to these fine sediments - into Maxwell Bay along the
cove’s shouthern coastline. Finally, always in light of the main water
circulation, the Creek area receives a lot of brash ice and ice flow from the
glacier. It is therefore likely that the assemblages at Creek station are
influenced by both, intermediate levels of terrestrial inorganic sedimentation
and ice disturbance.
Macrofaunal abundances were lowest at Creek with a patchy distribution
(Fig. 9 b), possibly related to the diverse impact of both, melt water and ice.
Thus, relatively younger and smaller individuals of Y. eigthsi (shell length <
1–1.5 cm) were present at Creek compared with Faro (> 2 cm). Despite the
high abundance of Y. eightsi, the scavenger/predator B. cristata was the
75
Chapter II. Spatial analysis
dominant biomass component at Creek. Likewise, a shift towards
smaller/younger Y. eightsi was observed at Signy Island after an iceberg
scour event (Peck and Bullough, 1993). The authors suggested that the
removal of adults, which inhibit the settlements of larvae, facilitates
recruitment in this bivalve species. The higher presence of vagile
scavengers like amphipods or the scale worm B. cristata are also indicative
of ice growler impact, as they feed on decaying animal material (Smale
2007, Smale 2008). Although the level of disturbance at Creek station is
very high, a low number of small sized filter and suspension feeders were
observed, indicative of sufficient near bottom currents with intermediate
turbidity caused by melt water and wave action.
Fig. 11 Conceptual scheme of the cove’s processes. For details see legend on figure.
Sites are given in an order such that it reflects the clock-wise direction of the current
entering the bay from west (see white ondulated arrow in the figure with main current
direction).
Prokaryotes at Creek were relatively abundant, probably taking advantage
of the high BPC and primary producers as inferred from Chl-a
concentrations. The meiofaunal densities were similar to those found at Isla
D and higher than at Faro. The distribution of meiofauna, as deduced from
the nMDS, shows similarities with Isla D, and is more scattered than in Faro,
probably indicating a higher micropatchiness within these sediments. At
76
Chapter II. Spatial analysis
Creek and, to a lesser extent, at Faro macrofaunal biomass was relatively
higher than that of prokaryotes and meiofauna, which suggests that C org
was more efficiently transferred to higher trophic levels here, maybe
through a shorter food chain dominated by scavengers/predators. The
nematode assemblage at Creek was relatively diverse and characterized by
the highest number of genera (21). The trophic diversity was evenly
structured with non-selective deposit feeders being dominant, closely
followed by epistrate feeders and a higher proportional presence of
predators. No genus dominated at this site, which indicates that this
assemblage is well adapted to the local disturbance regime.
5.
Conclusions
A summarizing conceptual scheme of the processes in the cove is
presented in Fig. 11. The distribution of the different components involved in
the benthic system (microbiota, meio- and macrofauna) varies in response
to a complex array of variables. In general, it is clear that different
assemblages (in terms of abundance, biomass and trophic structure) exist
at a same depth over a relatively small spatial scale (about 1 km 2) within the
same cove water body. Moreover, our results suggest that the size-class
specific life history traits of organisms may allow them to respond in diverse
ways to glacier related disturbance. Where the glacier influence is generally
low (Faro station) a macrofauna assemblage with an even biomass
distribution of different trophic groups was found, while higher organic
matter concentrations can accumulate in the sediments with consequences
for hypoxia sensitive meio- and microbiota (e.g. hypoxic sediment
conditions). Ice growler action is likely reflected in the high patchiness of
the soft bottom benthos at stations Creek and Isla D, with dominance of a
motile fauna and a virtual lack of sediment sessile species, together with the
higher relative abundance of fast spreading nematode colonizers such as
Microlaimus. It is likely that with time, once the glacier will have redrawn
completely onto the land ice scour will cease and the re-establishment of
more diverse and less patchy distributed macrobenthic assemblages can
be expected. Anyhow, future repeated samplings are needed in order to
confirm these conclusions and substantiate our present observations and
predictions.
6.
Acknowledgments
We acknowledge the ESF IMCOAST project (Impact of climate induced
glacial melting on marine coastal systems in the Western Antarctic
77
Chapter II. Spatial analysis
Peninsula region, www.imcoast.org), the vERSO project (Ecosystem
Responses to global change: a multiscale approach in the Southern Ocean,
funded by the Belgian Science Policy Office, BELSPO, contract
n°BR/132/A1/vERSO) and the Progetto Antartide PNRA 2010/c1.03 for
financial support. The first author was financed through an IWT PhD
scholarship and by Ghent University. We also thank the Instituto Antartico
Argentino (Argentina) for providing the logistics at Dallmann laboratory in
Carlini station. A special thank goes to Oscar González for his assistance
and logistic support. We would like to thank all the scientific and military
staff of Carlini station for the collaboration in the diving and boat activities
necessary for the collection of the here presented material. The merit of the
drawing we present as conceptual scheme goes to Dr. Hendrik Gheerardyn
(www.hendrik gheerardyn.com). We like to thank Dr. Mathias Braun for
supplying the detailed map including the glacier retreat lines. Finally we
would like to express our gratitude towards two specialists in the field:
Natalia Servetto (Universidad Nacional de Córdoba) who helped identifying
the sea pen Malacobelemnon daytoni and Dr. Katrin Linse (British Antarctic
Survey) for the identification of Mysella charcoti. And last but not least, we
would like to thank Dr. Dan Smale and Dr. Julian Gutt for their valuable
comments and vital contributions in ameliorating this work.
78
Chapter III. Trophic interactions
A curious fur seal (Arctocephalus gazelle) among a moss field at sunset
"Many times I have thanked God for a bite of raw dog."
Robert Peary
(1856-1920)
Chapter III. Trophic interactions
Adapted from:
Pasotti, F., Saravia, L.A., De Troch, M., Tarantelli, M.S., Sahade, R. and
Vanreusel A.: Benthic trophic interactions in an Antarctic shallow water
ecosystem affected by recent glacier retreat, Biogeosciences, submitted,
2014.
Abstract
The West Antarctic Peninsula is experiencing strong environmental changes
as a consequence of the ongoing regional warming. Glaciers in the area are
retreating at a fast pace and increased meltwater and inorganic
sedimentation runoff threatens the benthic biodiversity at shallow depths.
We identified three sites with a distinct glacier-retreat related history and a
different glacial influence in the inner part of Potter Cove (King George
Island, West Antarctic Peninsula), a fjord like embayment impacted since
the 1950’s by a tidewater glacier retreat. We compared the meio- and
macrofauna isotopic niche widths (δ13C and δ15N stable isotope analysis) at
the three sites to investigate possible glacier retreat influences on the
benthic trophic interactions. The isotopic niches appeared to be locally
shaped by the different degrees of glacier retreat-related disturbance
observed within the cove. The retreat of the glacier seems to favor wider
isotopic niches lowering initial local competition. The retreat of the ice is
known to provide for new available resource pools via macroalgae
colonization and likely enhanced sea ice algae sedimentation. An
intermediate and continuous state of ice-disturbance (e.g. ice-growlers)
allows new species and new life strategies to settle during repeated
colonization processes. The smaller benthic organisms (e.g. meiofauna)
seemed to be the primary colonizers of these disturbed sediments, showing
a wider isotopic niche. Ice-scour and glacial impact can play a two-fold role
within the cove: i) they either stimulate trophic diversity by allowing
continuous re-colonizations of meiobenthic species or, ii) in time, they may
force the benthic assemblages into a more compacted trophic structure
with increased level of connectedness and resource recycling. In general
the high degree of omnivory feeding common among the studied benthic
organisms represent an evolutionary functional buffer against a wide array
of environmental stressors and it is likely to help the benthos in coping with
climate change and related glacier retreat.
Keywords: macrofauna, meiofauna, stable isotopes, food web, West
Antarctic Peninsula,King George Island
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Chapter III. Trophic interactions
1.
Introduction
The West Antarctic Peninsula (WAP) is one of the Earth’s most rapidly
warming regions over recent decades (Anisimov and Fitzharris, 2001;
Convey et al., 2009a; Thomas et al., 2013; Vaughan et al., 2003), with
obvious consequences such as ice-sheet thinning (Pritchard et al., 2012),
widespread retreat of glacier fronts (Cook et al., 2005), retreat and collapse
of ice-shelves (Cook and Vaughan, 2009; Scambos et al., 2004) and
acceleration of snow melting (Abram et al., 2013). The warmer air
temperatures lead to rapid local increases, during the summer months, in
glacial melt and discharge (Dierssen et al., 2002) and enhanced snow and
permafrost melting (Abram et al., 2013). In the coastal marine environment,
these two processes are responsible for changes in water column turbidity
and stratification (Dierssen et al., 2002; Schloss et al., 2002), local
increases in inorganic sedimentation (Eraso and Dominguez, 2007), the
appearance of newly available ice-free substrata (Gryziak 2009: IlievaMakulec and Gryziak 2009; Favero-Longo et al., 2012; Quartino et al.,
2013), and changes in the frequency and scale of ice disturbance (Smale
and Barnes, 2008).
Disturbance is a key factor in structuring benthic communities worldwide
(Barnes and Peck, 2008; Barnes and Souster, 2011; Barrett et al., 2008;
Schratzberger et al., 1999). In the Antarctic, one of the major structuring
forces involved in shaping the shallow benthos is ice scouring (Brown et al.,
2004; Convey et al., 2012; Gutt, 2001; Lee et al., 2001a; Sahade et al.,
1998b; Smale and Barnes, 2008; Smale, 2007), including the formation of
anchor ice (Denny et al., 2011; Sahade et al., 1998b). Other factors such as
sedimentation have been seen to affect Arctic meio- and macrobenthos
distribution (Wlodarska-Kowalczuk and Weslawski, 2001; Grzelak and
Kotwicki, 2012; Grange and Smith, 2013), Antarctic soft coral survival (after
a slumping event, Slattery and Bockus, 1997), and the physiology and
survival of Antarctic key species such as the bivalve Laternula elliptica,
ascidians and the sea-pen Malacobelemnon daytoni (Husmann et al., 2012;
Philipp et al., 2011; Torre et al., 2012, 2014). The potential crossing of
sedimentation and meltwater input thresholds as climate change advances
in the West Antarctic has been denounced as a big threat to fjords
biodiversity hotspots (Grange and Smith, 2013). However a positive feature
of this process is the availability of newly ice-free substrata that may
stimulate new colonization and initiate succession processes, as recently
documented for Antarctic marine (Gutt et al., 2011; Quartino et al., 2013;
Raes et al., 2010) and terrestrial ecosystems (Convey, 2011; Favero-Longo
et al., 2012; Gryziak, 2009; Ileva-Makulec Krassimira and Grzegorz, 2009).
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Chapter III. Trophic interactions
Although not unique in the history of the West Antarctic Peninsula (Thomas
et al., 2013), these rapid ongoing environmental changes can be
considered as a perturbation to the most recently natural disturbance
regime that Antarctic shallow marine communities were used to experience.
Such changes, therefore, constitute potential stress factors that may alter
community composition and species interactions.
Studies on the influence of glacier-related effects on the benthic biota have,
so far, been focused on the investigation of individual species responses
(Philipp et al., 2011; Torre et al., 2012), or on the description of benthic
community structure (Brown et al., 2004; Grange and Smith, 2013; Pasotti et
al., 2014a; Sahade et al., 1998b, 2004). Moreover, important shifts in macroepibenthic communities structure were as well related to increased glacial
influence at Potter Cove (Sahade et al., in prep.), pointing to the necessity
of including also communities functional responses to the changing
process. Although there are already a few food web studies that describe
the Antarctic benthos trophic relationships (Corbisier et al., 2004; Gillies et
al., 2013, 2012; Kaehler et al., 2000), no study has attempted yet to link
possible local glacier retreat and related environmental conditions to
differences in benthic trophic interactions.
Fig. 1 Map of Potter Cove and its location within the Antarctic (from Pasotti et al.,
2014b and with the courtesy of Dr. Mathias Braun). The history of the retreat of the
Fourcade glacier is illustrated with the ice front position lines for each specific year.
In the present study, we aimed at investigating in detail the trophic structure
of three assemblages experiencing different local conditions in respect to
the ongoing glacier retreat and the overall Potter Cove food web. The cove
has experienced glacier retreat since the 1950s, exposing new ice-free
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Chapter III. Trophic interactions
substrata (Rückamp et al., 2011). Based on observations in three shallow
stations in Potter Cove, Pasotti et al. (2014b) recently showed how
community structure of the benthos (microbiota, meio- and macrofauna)
varied along a virtual line of “age-since glacier retreat” and the distance
from the current glacier front. The most recent ice-free area was strongly
influenced by glacier retreat (e.g. via ice growlers action or because of high
sediment accumulation rates) and showed a more patchy benthic
assemblage with lower overall biomasses dominated by scavengers and
motile taxa. Higher biomass of benthos was reported from the site of
intermediate ice-free age and experiencing strong wave action. Focusing
on exactly these sites within Potter Cove, we wanted to understand whether
the documented time-space integrated glacier retreat consequences
observed on the assemblage structures (Pasotti et al., 2014b, Chapter II of
this thesis) could also be observed at the level of their trophic interactions
and overall food web structure and therefore be reflected into their isotopic
niche distribution (e.g. given by the organisms positions within the δ13C-δ15N
bi-plot space). We analysed dual stable isotopic signatures (δ13C and δ15N)
of two benthic size classes (meio- and macrofauna).
2.
Material and Methods
2.1. Study site
Potter Cove is a small fjord-like bay at the southern coast of King George
Island (South Shetland Islands, Fig. 1). The cove is characterized by the
recent retreat of the Fourcade glacier (Rückamp et al., 2011). Additional
freshwater input originates from seasonal meltwater discharge as a
consequence of permafrost and snow melting processes. The three shallow
water (15 m) stations included in the present study (see Fig. 1) are located
in the inner part of the cove and are mainly characterized by soft sediment
(Pasotti et al., 2014a,b). Isla D station (62° 13' 32.6" S, 58° 38' 32" W) is the
most recently ice-free area (2003-2006), and is situated closest to the
glacier front. Faro station (62° 13' 32.6" S, 58° 40' 03.7"W) lies near the
northern shore of the cove and became ice-free between 1988 and 1995.
The site is further characterized by higher bed shear stress (Wölfl et al.,
2014). Creek station (62° 13‘57.3" S, 58° 39’ 25.9" W) is located adjacent to
a seasonal meltwater river (“Potter Creek”) and is ice-free since the early
1950’s. The three sites present distinct benthic communities and biomasses
despite their relative vicinity (Pasotti et al., 2014b) and these differences
have been related to the glacier retreat history. Isla D and Creek, were the
sites affected by ice growlers action and by higher inorganic sedimentation.
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Chapter III. Trophic interactions
Isla D was the site with the highest sediment accumulation rates. More
details on the benthic assemblage composition are given in Pasotti et al.
(2014b).
2.2. Sampling and stable isotope analyses
Samples for stable isotopes analysis were obtained during two campaigns
in February/March 2011 and March 2012, respectively (Pasotti et al.,
2014b). The majority of potential food sources were sampled during the first
campaign, whilst microphytobenthos could only be collected during the
second season. Meiofauna and macrofauna were mostly collected during
the first campaign. From the second sampling campaign in March 2012,
two cumacean species collected at Isla D and polychaetes (suborder
Terebellida, family Ampharetidae) were added to the dataset. The majority
of collected organisms were stored in formaldehyde (see further), with the
remainder being stored frozen (-20°C) prior to stable isotope analyses. In
view of the depleting effect of formaldehyde on background stable isotopic
carbon signatures (Kaehler and Pakhomov, 2001; Rennie et al., 2012;
Sarakinos et al., 2002), we applied a correction factor of +2‰ to the δ13C
values (Rennie et al., 2012) of those invertebrate samples that were stored
in formol and processed within 6 to 12 months of sampling. No lipid
extraction was applied to the samples. The dual isotopic composition
(carbon and nitrogen) of the samples was analyzed with a PDZ Europa
ANCA-GSL elemental analyzer 230 interfaced to a PDZ Europa 20–20
isotope ratio mass spectrometer (Sercon Ltd., Cheshire, UK; UC Davis
Stable Isotope Facility, http://stableisotopefacility.ucdavis.edu/). All isotope
data were expressed in standard δ notation (measured as ‰), comparing
the ratio of the heavy/light isotope to standard reference materials (Pee Dee
belemnite for carbon and atmospheric N2 for nitrogen). All organisms were
washed with milliQ water (when applicable) and dried overnight at 60°C.
After drying the material was grounded to a fine powder by means of a
mortar and placed in Al (for dual - δ13C and δ15 N – or solely δ15N analysis)
or Ag (for δ13C analysis when acidification was required) capsules (6.5 * 8
mm). In the latter case, all carbonates were removed prior to the δ13C
analysis through acidification with “drop by drop” addition of HCl of specific
concentrations (see details below). All capsules were dried pinched closed
and kept dry until further analysis.
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Chapter III. Trophic interactions
Suspended Particulate Matter (SPM)
Water column SPM data were obtained from the work of Tarantelli et al. (in
prep.). Water samples were taken with Niskin bottles from 0 to 30 m depth
at the inner and the outer cove during the austral summer 2007-2008 and
2008-2009. The water samples were filtered with GF-F glass fiber filters (47
mm diameter, 0.7 μm porosity), treated drop by drop with 1 M HCl and
rinsed with distilled water to eliminate carbonates. Lipids were extracted in
Chloroform-methanol (2:1 vol : vol). The isotopic analysis was performed in
a mass spectrometer (IRMS) Thermo Finnigan Delta XP Plus connected by
a Thermo Finnigan Conflo III to an element analyzer Thermo Flash EA 1112.
Phytoplankton and Zooplankton
For zooplankton and phytoplankton samples, seawater was filtered during
horizontal tows (0-15 m, 15 min) with 220 μm and 55 µm mesh nets at each
study site within the cove, but considered as belonging to no site in light of
the short distance in between the stations and the current system within the
cove. Each sample obtained was filtered on pre-combusted (500°C for 2h)
GF/F glass fiber filters (47 mm diameter, 0.7 μm porosity). Filters were
stored frozen (-20°C) until further analysis. During the processing of
microalgal material, eachfilter was examined under a dissection microscope
and any zooplankton present was hand-picked and removed from the filter.
The microalgae were then gently scooped from the filter with a sterile
spoon-tipped needle and placed into the capsules. For zooplankton, only
calanoid copepods and one large individual mysid provided sufficient
biomass for dual stable isotope analysis.
Sediment
Sediment samples were obtained via scuba diving by means of perspex
push cores (5.6 cm inner diameter) at each site (2 replicates per site). One
centimeter slices were cut from the surface down to 5 cm depth of sediment
and stored into petri dishes (diameter 90 mm). Samples were kept frozen (20°C) prior to further analysis. From each layer of each core, aliquots of
sediment were taken for δ13C and δ15N stable isotope analysis. Sediment
aliquots were acidified (in Ag capsules) with increasing concentrations of
HCl (0.25 N, 1 N, 2 N) in order to avoid excessive bubbling and loss of
sediment.
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Chapter III. Trophic interactions
Microphytobenthos
Sediment with a brownish microphytobenthic layer was sampled via scuba
diving with the use of perspex push cores (5.6 cm inner diameter).
Immediately after sampling, the top centimeter of sediment was separated
and stored in a Petri dish placed into a tray filled with ice in order to prevent
pigment degradation. In the laboratory, microalgae were extracted from the
sediment by placing lens tissue on its surface under an artificial light. Glass
cover slips placed on top of the lens tissue were used to collect the
microalgae migrating towards the light and adhering to the cover glass. The
microalgal biofilm was then scraped off the slide, collected with pre-filtered
seawater and filtered on a GF/F (pre-combusted 550°C) filter and stored
frozen (-20°C) until analysis. At the time of preparation for the dual stable
isotope analysis, the filter was placed under a dissecting microscope and
the visible microalgal mat was carefully scooped with a spoon-like needle
from the surface of the filter.
Macroalgae
Specimens of seven representative algae species (see Table 1) were handcollected by scuba divers on the northern rocky shore of the cove, where
macroalgae are most abundant (Quartino et al., 2013). The specimens were
washed repeatedly with milliQ water and dried at 60°C for 48 h. The dried
material was stored in Petri dishes and kept dry until further processing.
During the processing, small sections of the dried algae were homogenized
with a mortar and destined to the analysis.
Meiofauna
Sediment cores (5.6 cm inner diameter) were collected at each station by
scuba diving, sliced as described in section 2.2.III, and stored in 4%
formaldehyde (buffered with pre-filtered sea water). Initial dual stable
isotope analyses of nematodes, copepods and cumaceans from the
formalin (4%) samples did not provide reliable dual stable isotope values
and were therefore excluded from the analysis, whereas those of
polychaetes and amphipodes were used during the analysis. An extra
replicate was therefore processed to gather material for nematodes,
copepods and cumaceans. We sacrificed one replicate of the samples
collected for sediment analysis (0-1 cm layer, stored -20°C), hence a frozen
sample. Meiofaunal extraction followed standard procedures including
centrifugation with LUDOX HS40, and sieving over 1000 and 32 µm sieves
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Chapter III. Trophic interactions
(Heip et al., 1985, 1974). Extraction with LUDOX is known not to influence
the natural stable isotopic signatures of metazoans (Moens et al., 2002).
Meiofauna were identified at higher taxon level following (Higgins and Thiel,
1988) and the most abundant groups (nematodes, copepods, cumaceans,
polychaetes and amphipodes) were separated for stable isotope analysis.
For nematodes, 600 individuals were picked at random, washed repeatedly
in milliQ water and filtered on pre-combusted (500°C) GF/F glass fiber filters
(47 mm diameter, 0.7 μm porosity).
Harpacticoid copepods (40 individuals) were sorted into two morphotypes
(MT) in light of their morphology (e.g. belonging to different
families/genera): MT2 carried epibiotic ciliates on the exoskeleton.
Cumaceans and polychaetes were grouped, when possible, at the
family/species level. Cumaceans were acidified with 0.25 N HCl prior to
further δ13C analysis.
Macrofauna
The macrofauna were sorted into two size classes (see Table 1). The
endo/epibenthic organisms smaller than 1 cm were classified as “smaller
macrofauna” (e.g. Cirratulidae polychaetes, amphipodes etc.), and those
larger than 1 cm (e.g. Yoldia eightsi, Malacobelemnon daytoni) were
classified as “bigger macrofauna”.
In order to collect the “smaller” endobenthic and some of the “bigger”
macrofauna (e.g. Y. eigthsi, M. daytoni, Barrukia cristata, Aglaophamus
trissophyllus), sediment samples were obtained at each site by means of a
Van Veen grab operated from a zodiac. The sediment was washed over a 1
mm mesh sieve and the animals were sorted alive. The samples were
stored in 8% formaldehyde (buffered in pre-filtered seawater). At the time of
sample preparation, when possible, polychaetes were grouped to
family/species level or morphotypes, and amphipods and cumaceans were
sorted to family or species level. Small crustaceans were treated, prior to
drying, with 2N HCl to remove carbonates. In small taxa, several individuals
were used for isotopic analysis (see Table 1 for number of individuals used
per taxon and number of replicates used per analysis). Large mollusks (e.g.
Y. eightsi) were removed from their shells and muscular foot tissue from
individual organisms was collected. The internal calcareous rod of M.
daytoni was removed from the colony soft body tissue and part of the
colonial organism was dissected and carefully rinsed with milliQ water.
Samples were acidified with 2N HCl. Given their previously recorded
importance at this study site (Momo et al., 2002; Pasotti et al., 2014a,
2014b; Sahade et al., 1998a, 1998b), selected “bigger” macrofauna were
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Chapter III. Trophic interactions
hand-collected by divers in the vicinity of the studied sites, including the
isopod Paraserolis polita and the ascidians Molgula pedunculata,
Cnemidocarpa verrucosa and Corella eumyota. Upon collection these
organisms were left overnight in pre-filtered seawater in order to allow gut
clearance. The crustacean was frozen in liquid N 2 and stored at -20°C until
processing and analysis, whereas the ascidians were stored in formol (8%
final concentration). The muscle tissue from P. polita was removed by
means of a sterilized bistoury. For the processing of the ascidians, the tunic
of each individual ascidian was carefully dissected and rinsed in milliQ
water. Epiphytic bryozoans were present on the outer tunic of one specimen
of C. eumyota. The bryozoan was carefully removed and prepared
separately for stable isotope analysis (samples were acidified in 0.25 N HCl
prior to δ13C analysis).
2.3. Data analysis
We identified a total of 12 trophic groups as relevant for the benthic
interactions under study. Potential food sources were classified into 6
groups: SPM, phytoplankton 55 µm, phytoplankton 200 µm, macroalgae,
microphytobenthos (MPB) and sediment. Consumer taxa were classified
into the feeding groups of zooplanktonic grazer (Zoo), filter/suspension
feeder (Fi/Su), deposit feeder/omnivore (De/O), bearing epibiont (Epi),
scavenger/omnivore (Sc/O) or predator/omnivore (Pr/O) based on life traits
reported in available literature (see Table 1). In order to allow a description
of the community in terms of trophic levels (TL), we identified baseline
estimates of trophic position following McCutchan et al. (2003), Post (2002)
and Vander Zanden and Rasmussen (2001) and based on both our data
observations and literature background information on species traits. Food
sources showed a rather wide range of δ15N values, overlapping with
consumers values. We identified therefore the range of the first level of
consumers (TL2) of our food web based on the knowledge of the feeding
habits and life history traits of the investigated filter feeders and the longlived deposit/suspension feeder Yoldia eightsi. The protobranch bivalve
mollusk Y. eightsi represents an important component in terms of biomass
at our sites (Pasotti et al., 2014b). The organisms used during our
investigation were between 2-3 cm in length and hence likely older than 50
years (Peck and Bullough, 1993). Y. eightsi is known to be both a deposit
feeder (on mud) and a suspension feeder (on diatoms in the ventilator
stream) (Davenport, 1988), but in our analysis it was included in the deposit
feeder/omnivore (De/O) category owing to its sediment-related functional
characteristics. Based on Yoldia eightsi carbon signature data which seems
to be pointing to an influence of microphytobenthos in its diet, we included
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Chapter III. Trophic interactions
Y. eightsi in the second trophic level or in the first consumers cathegory.
Sea pens are known to be passive suspension-feeders of phytoplankton
(Best, 1988) and potentially very small zooplankton (Kozloff, 1990).
Bryozoans are also filter-feeders that feed on small phytoplankton (Ruppert
and Barnes, 1994). Ascidians in Potter Cove have been found to contain
macroalgal fragments in their gut (Tatián et al., 2004), besides potentially
feeding on phytoplankton and other particulate organic matter present in
the water column. We considered the benthic-pelagic compartment as one
single food web in light of the frequent re-suspension events in PC shallow
waters (Pasotti et al., 2014b; Schloss et al., 2002), which permit suspension
and filter feeders to potentially feed on both compartments at the same
time, given their non-strict feeding selectivity. We then decided to use a
double approach: i) for the next trophic (TL3-TL5) levels we decided to use
an intermediate δ15N trophic fractionation step derived from the McCutchan
et al. (2003) invertebrate-based and plant-based fractionation steps of
1.8‰ and ii) secondly we used the standard δ15N trophic fractionation of
3‰ (Post, 2002; Vander Zanden and Rasmussen, 2001).
We identified the trophic positions based on this information and making
use of the formula:
i)
TP = λ + (δ15N consumer - δ15Nbase) / Δn. (Post, 2002)
Where TP = trophic position of a particular species/group, λ is the trophic
position of the chosen organism used for the estimation of δ15Nbase (e.g., λ =
2 for primary consumers, 3 for secondary consumers), δ15N consumer is
measured directly, and Δn is the trophic enrichment (Δ15N, ‰) per level. We
identified two food webs of different lengths: i) a food web with a total of
four trophic levels of consumers and ii) a food web with three consumer
levels. Implications are discussed.
By means of Standard Ellipse Areas (SEAs, Jackson et al., 2011; Syväranta
et al., 2013) and Layman’s metrics (Layman et al., 2007), we compared the
three shallow benthic assemblage isotopic niches in relation to the ongoing
glacier retreat. In order to compare the benthic community isotopic niches
at the three sites (“by site”) or between the three size classes at each site
(“size by site”), we used Standard Ellipse Areas (SEA; expressed in ‰2;
Batschelet, 1981). SEAs are comparable to the univariate standard
deviation (SD) and contain about 40% of the variability of the dataset
(Batschelet, 1981). They are also more appropriate for unbalanced datasets
and allow comparisons between communities with different numbers of
taxa/groups (Jackson et al., 2011). Two Bayesian approaches were used to
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Chapter III. Trophic interactions
graphically represent the estimated (posterior) distribution of SEAs: i) the
representation of the probability of data distribution was calculated taking
into account uncertainty derived from the sampling process (SEA b; Jackson
et al., 2011) and ii) the data distribution was represented by applying a
correction for small sample size (SEAc; Jackson et al., 2011). All analyses
were completed using the SIBER package (Stable Isotope Bayesian
Ellipses in R; Jackson et al. 2011) within the SIAR package in R (Parnell and
Jackson, 2013). The R scripts used for the analysis are available at
http://dx.doi.org/10.6084/m9.figshare.1094784. We tested normality with the
multivariate Shapiro-Wilk test and graphically with quantile-quantile plots in
R (data not shown). One of the three sites did not meet the normality
assumption but, since each of the datasets has sample size of n ≥ 30, SEAc
is robust to this violation (Syväranta et al., 2013). In “size by site” analysis
three out of nine data distributions did not follow normality and the sample
size was < 30 (n ~ 10), hence we could not use SEA c to compare the
overlaps. We tested the Bayesian model using a simple graphical method:
we plotted together the single SEAc and the SEAb distribution. The metric
calculated from the data (as single point SEAc) must lie inside the 95%
credible intervals calculated from the Bayesian analysis (McCarthy, 2007).
In addition, we compared the three sites in terms of trophic structure using
the community-wide metrics of Layman et al. (2007). These metrics were
suited for comparison of the three sites in this study since the food source
δ13C ranges were the same (Jackson et al., 2011). The same Bayesian
approach was used to incorporate uncertainty and allow comparison of
posterior probabilities. We calculated five metrics using groups defined as
size classes (Table 1): (i) δ13C range (CR), indicative of niche diversification;
(ii) δ15N range (NR), indicative of trophic length; (iii) mean distance from
centroid (CD), indicative of the average trophic diversity; (iv) mean nearest
neighbor distance (MNND), or a measure of the density of species packing;
and (v) standard deviation of mean nearest neighbor distance (SDNND), or
evenness of species packing. Together the last two metrics are indicative of
trophic redundancy: small MNND indicated higher trophic redundancy,
where more species perform the same trophic function, and lower SDNND
indicates more evenly distributed species with more species having similar
ecological traits.
For the analysis we ran the SIBER analysis on two sets of datasets: i) the
main analysis based on the complete dataset (“complete dataset”) which
forms the core of the chapter, where we merged all the possible information
on the three sites and used all the available samples, and ii) the analysis
without “ambiguous” data where we excluded possible outliers or species
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Chapter III. Trophic interactions
not found during the qualitative sampling for stable isotope analysis but
known to be usually present at the investigated sites (as from Pasotti et al.,
2014b). From the “reduced dataset” we excluded from Isla D i) the
harpacticoid copepod MT2 since this species could be seen as an outlier
(very depleted δ13C and δ15N values) and ii) the two polychaete species
Barrukia cristata (Polynoidae) and Aglaophamus trissophyllus (Nepthydae),
since they were found during the qualitative sampling only at Creek station.
Nevertheless, since Pasotti et al. (2014b) reported that these two
polychaete species represented an important component of the Isla D
benthic community in the summer 2011 and in light of the metabolic
peculiarity of the very depleted values of the copepod MT2, we included
these organisms in Isla D in the”complete analysis” and based our detailed
results and main discussion on this analysis.
3.
Results
Results are expressed in mean± SD.
In the section 3.2. “Inter-site comparison: spatial differences in trophic
structure” we report in detail results from the SIBER “complete dataset”
analysis. In the Addendum the results from the “reduced dataset” analysis
are resumed in three tables (Table A4 “by site” analysis; Table A5 “size by
site” analysis: Table A6 Layman’s metrics analysis) together with the results
of the “complete dataset” analysis for direct comparison. The complete set
of figures is included in the Addendum (Fig. A1- Fig A4) to avoid the
chapter to result too bulky. At the end of the discussion a section is
dedicated to the discussion of such analysis on the overall interpretation of
the “complete dataset” analysis.
3.1. Stable isotope signatures
Mean dual stable isotope values and standard deviations (± SD) of the taxa
are summarized in Table 1. The list of taxa with their trophic group and
trophic levels (TL) for each of the calculated food webs is reported in Fig 2
(A four consumer TLs; and B three consumer TLs). The δ13C values are
presented in Fig. 3 and the single point data bi-plot (in the δ13C/ δ15N
space) is represented in Fig. 4. The food sources ranged from the more
depleted carbon isotopic values of macroalgae (mean δ13C: -25.03‰ ±
5.45) and SPM (mean δ13C: -26.08 ± 1.17 ‰), to the rather enriched values
of MPB (mean δ13C: -13.15‰ ± 0.35). SPM showed overlapping δ13C
signatures with phytoplankton 200 µm and macroalgae. Macroalgae
showed the widest range of δ13C values. In terms of δ15N signatures SPM
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Chapter III. Trophic interactions
showed the most depleted values (0.45‰ ± 1.17) whereas the other food
TL ranged around 3-4‰. For the consumers, the deposit feeder/omnivore
(De/O) feeding group showed the widest range of δ13C values (-17.82‰ ±
2.57), followed by scavenger/omnivore (Sc/O, -16.76‰ ± 1.79),
predator/omnivore (Pr/O, -16.70‰ ± 1.74), zooplankton (Zoo, -23.80‰ ±
1.41) and filter/suspension feeder (Fi/Su, -23.51‰ ± 0.95 SD). The most
depleted δ13C (-34.9‰) as well as δ15N (-2.6‰) values were recorded for
the harpacticoid copepod MT2 which was the taxon present at Isla D
colonized by epibionts (likely ciliates). δ15N values of consumers showed a
similar pattern with De/O presenting an intermediate position in the trophic
level bi-plot (Fig. 3) representing all the consumer trophic levels and
showing therefore the widest range of δ15N signatures (8.96‰ ± 2.18). The
Fi/Su occupied the lower trophic level (TL2, δ15N 5.30‰ ± 1.17), whereas
Sc/O (10.17‰ ± 1.14) occupied the range of TL2-TL3 (Fig. 3A) and TL2-TL4
(Fig 3B)and Pr/O (11.86‰ ± 0.71) TL3-TL4 (Fig.3A and B).
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Chapter III. Trophic interactions
TL3
TL4
TL5
<--------TL2 range -- ----->
Barrukia cristata. (I + C)208
Priapulus sp. (F)204
Aglaophamus trissophyllus (I+ C)200
Paraserolis polita (F)196
Amphipods (I)192
Amphipods MT1 (F)188
Phoxocephalidae (F)184
Phoxocephalidae (C)180
Nematodes (C)176
Namatodes (I)172
Nematodes (F)168
164
Maldanidae MT2 (F)160
Maldanidae MT1 (F)156
Cirratulidae (F)152
Orbinidae (F)148
Cirratulidae MT2 (C)144
Cirratulidae MT1 (C)140
Capitellidae(F)136
Capitellidae (C)132
Capitellidae (F)128
Ophaelidae (F)124
Harpacticoid copepods MT1 (I)120
Harpacticoid copepods MT2 (I)116
Eudorella sp. (C)112
Eudorella sp. (F)108
Dyastilis sp. (I)104
Eudorella sp. (C)100
Eudorella sp. (I)96
Eudorella sp. (F)92
Spionidae (F)88
Cerratulidae (C)84
Cerratulidae (F)80
Yoldia eightsi (C)76
Yoldia eightsi (F)72
Nototanaid MT2 (F)68
NototanaidMT1 (F)64
Mysids60
Calanoid copepods56
Bryozoan (I)52
Cnemidocarpa verrucosa (I)48
Corella eumyota (I)44
40
Molgula pedunculata (I)36
Malacobelemnon daytoni (F)32
Sediment (C)28
Sediment (I)24
Sediment (F)20
MPB16
Macroalgae12
Phytoplankton 55 µm 8
Phytoplankton 200 µm 4
SPM 0
Predator
Omnivore
<-- Food source range -->
TL1
Scavenger
Omnivore
Deposit feeder
Omnivore
Epibiosis
Zooplanktonic
grazer
Filtersuspensionfeeder
Sediment
POM
Primary
producer
Δ15N = 1.8‰
SPM
-3
-2
-1
0
1
2
3
4
5
6
δ15N
7
(‰)
8
9
10
11
12
13
14
15
2a
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Chapter III. Trophic interactions
2b
Fig. 2 Stable isotope δ15N values of the two food webs (food web A Δ15N = 1.8‰; food
web B Δ15N = 3‰) with taxa trophic group designation. In the list of species/taxa,
where appropriate, the site where the organism was sampled is reported in between
brackets. Meiofauna taxa have been highlighted in bold. In green the baseline
organism Yoldia eightsi is highlighted. The abbreviations in the list are Creek = C;
Faro = F; Isla D = I; SPM = suspended particulate matter; POM = particulate organic
matter; MPB= microphytobenthos; TL = trophic level. Specification of the net mesh
size used to sample the phytoplankton is included in the list (55 µm or 200 µm mesh
size). Symbols are: closed dark circles = food sources; open squares = filtersuspension feeders; open triangles= deposit feeder/omnivore; open rhombus =
scavenger/omnivore; open circles = predator/omnivore.
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Chapter III. Trophic interactions
Fig. 3 Stable isotope δ13C values of food sources and consumers. In the list of
species/taxa, where appropriate, the site where the organism was sampled is
reported in between brackets. Meiofauna taxa have been highlighted in bold. In
green the baseline organism Yoldia eightsi is highlighted. The abbreviations in the list
are Creek = C; Faro = F; Isla D = I; SPM = suspended particulate matter; POM =
particulate organic matter; MPB= microphytobenthos; TL = trophic level.
Specification of the net mesh size used to sample the phytoplankton is included in
the list (55 µm or 200 µm mesh size). Symbols refer to trophic group designation as
from Fig. 2.
3.2 Inter-site comparison: spatial differences in trophic structure
Standard ellipse areas corrected for small sample size (SEAc) “by site”
showed differences in shapes and sizes between the sites (Fig. 5). Isla D
presented the most elongated and narrow shaped ellipse among the three
sites. It covered the largest SEA (23.11‰2), followed by Faro (19.88‰2) and
Creek (14.89‰2). The probabilities that the standard ellipse area (SEA b) of
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Chapter III. Trophic interactions
Isla D was larger than those of Faro or Creek were 87% and 98%
respectively (Fig. 6). The probability that the SEAb of Faro was bigger than
that of Creek was 90%. The overlap between Faro and Creek was larger
(11.92‰2) than between either Creek and Isla D or Faro and Isla D (6.19‰2
and 9.15‰2). respectively). A SEAc of the “site by size class” (Fig. 7, see
Addendum Table A5 for SIBER results) showed again more elongated and
narrow shaped ellipses at the Isla D site. The narrowest ellipses at this site
were due to the “meiofauna” (58.25‰2) and “bigger macrofauna” (11.38‰2)
size classes. Faro displayed a rounder, smaller and thus more compacted
ellipse in the “bigger macrofauna” size class (37.97‰ 2), whilst the
“meiofauna” and “smaller macrofauna” ellipses resembled each other in
terms of shape, but differed in terms of size (2.45‰2 and 15.37‰2
respectively). The three size classes at Creek showed similar SEA c ellipses,
both in shape and size (“meiofauna” 7.92‰2; “smaller macrofauna” 7.82‰2;
“bigger macrofauna” 11.65‰2), although the overlap could not be
compared due to small sample size. The probabilities that “meiofauna”
ellipses were larger than “smaller macrofauna” ellipses were 90% at Creek,
0% at Faro and 100% at Isla D. The probabilities that “bigger macrofauna”
ellipses were larger than “smaller macrofauna” ellipses were 95% at Creek
and 99% at Faro and at Isla D. In light of the possible “outlier effect” of the
very depleted signals of the harpacticoid MT2 (carrying a ciliate epiobiont)
at Isla D, we decided to repeat the SEAs analysis without including this
sample. However the same trend was confirmed, with Isla D showing the
larger SEAs among the three sites.
The Layman’s metrics are summarised in Fig. 8 (the Bayesian probability
tables are given in the Addendum, Table A6). In terms of distance (‰), Faro
showed the largest NR, with a 70% probability of being greater than Isla D
and 95% probability of being greater than Creek. The CRs of Creek and Isla
D were similar (Creek > Isla D = 56% probability), whereas Creek and Isla
D displayed larger CRs than Faro with 90% and 76% probability,
respectively. Redundancy at the three sites did not show strong differences.
The mean distance to centroid (CD) did not show significant differences,
with the Credibility Intervals (CI) overlapping between all sites. The mean
near neighbour distances (MNND) were relatively similar for the three sites,
and did not show significant differences. In fact the CI overlapped between
the sites (data not shown).
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Chapter III. Trophic interactions
Fig. 4 δ13C and δ15N bi-plot with food sources (full black symbols) and trophic groups (see legend for symbols) and stations (see
legend for colors). The consumers which did not belong to any site were presented in purple empty circles. “Bearing
ectosymbionts” refers to the harpacticoid copepod MT2.
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Chapter III. Trophic interactions
Fig. 5 Standard ellipse areas corrected for small samples size (SEA c, full lines) and
convex hul areas (dashedlines) for all sites.
6
Standard
ellipse area Bayesian
estimations
(SEAb)
with mode (black
dots) and probability
of data distribution
(50%
dark
grey
boxes;
75%
intermediate
grey
boxes; and 95% light
grey boxes) for each
site. The standard
ellipse area corrected
for small sample size
(SEAc)
is
also
presented as red
squares.
Fig.
.
97
Chapter III. Trophic interactions
Fig. 7 Standard ellipse area corrected for small sample size (SEAc) for each site with the three consumer size classes (see legend
for colors).
98
Chapter III. Trophic interactions
Fig. 8 Community wide metrics for the three sites (see legend for colors). The dark
squares are the mode, the triangles the Bayesian probability and the bars represent
the 95% credibility interval of the posterior probability distribution. NR = Nitrogen
range; CR= Carbon range; CD= mean distance from centroid; MNND= mean nearest
neighbour distance; SDMNND= standard deviation MNND.
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Chapter III. Trophic interactions
4.
Discussion
4.1. Temporal and spatial glacier retreat effects on benthic trophic
interactions
In the following three paragraphs we will discuss the main results (from the
“complete dataset” analysis) of this work observing the spatial pattern first
at the site level, then within each investigated size class at each site. We will
then expand these considerations in respect to the ice-free age of the sites.
A fourth paragraph will be dedicated to presenting the general highlights
observed during the “reduced dataset” SIBER analysis. Finally we will draw
some general conclusions on Potter Cove benthic food web structure.
Spatial patterns: isotopic niche width
By a comparison of the three distinct study sites representing different
glacier retreat dynamics, clear differences were observed suggesting that
the SEAc shapes mirror the history of these assemblages in relation to the
glacier retreat timing. In fact, the degree of compaction of the three isotopic
niches under study showed differences in line with the ice-free age status of
each site, and the associated environmental conditions at the time frame of
sampling. The most recent ice-free station (Isla D) presents the less
compact and the wider isotopic niche available, whereas the site which is
known to be ice-free since the longest time (Creek) has the most
compacted SEAc shape.
In addition to local environmental differences (see discussion below) which
can explain this observation, it is worth noting that this trend could be due
to the ability of these Antarctic benthic assemblages to increase their
degree of interconnectedness within the food chain during the short (years
to decades) time that passed since the newly ice-free status was achieved,
exhibiting a remarkable capacity to adapt to the strong ongoing climatedriven changes.
In fact, the three sites under study can be considered as a time-integrated
snapshot of glacier retreat effects on shallow water benthic trophic
organization. Situated at the same water depth and within a distance of
about one kilometer among them, the benthic communities of the three sites
have been shaped in relation to the glacier front dynamics as well as by the
local conditions (Pasotti et al., 2014b). Since the 1950’s the glacier has
been actively retreating, exposing the previously underlying sediments to
the open water, seasonally loaded with high inorganic sedimentation.
Moreover, summer ice growlers detaching from the calving glacier have
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Chapter III. Trophic interactions
been ploughing with variable frequency the shallow bottoms of the three
sites at different moments during the history of this glacier retreat. Following
the observations of Rückamp et al. (2011), we could identify Creek as the
first of the studied locations to become ice-free (in the early 1950’s). Due to
its location, the conformation of the glacier and the clock-wise current
system of Potter Cove, the site is the one which experienced the stressors
of the glacier retreat for the longest time. In fact, the site still experiences
ice impact as well as glacial meltwater discharge during summer months.
Faro station became ice-free over a time span of about 7-8 years around
the 90’s. During this time period the glacier was reaching very near to this
newly ice-free island and the benthic assemblage likely suffered of
inorganic load, drop stones and ice growler impact for a prolonged period.
Nowadays Faro site seems to be the least affected by ice growlers impact
(Phillip et al., 2011) and it shows the lowest sediment accumulation rates
but high bed shear stress (Wőlfl et al., 2014). The most recent newly ice-free
area (2003-2006) is that surrounding Isla D site. Isla D station reports the
highest sediment accumulation rates among the three sites, and it is still
highly affected by ice impact as reflected in the patchy distribution of the
endobenthic assemblage (Pasotti et al., 2014b). The sediments of the three
sites may have possibly been already inhabited prior to the calving of the
Fourcade glacier and if we compare to what was already documented for
other pre-ice-shelf-collapse benthic assemblages (Gutt et al., 2013; Raes et
al., 2010), local communities might have been more impoverished in terms
of abundances and/or diversity when under the ice, especially for the more
inward site Isla D which is the most recently ice-free. This site in fact
presented the largest isotopic niche width, and having been for the longest
time under the glacier compared to the other two sites, the local benthic
assemblage here may have undergone a successional process where
competition for niche space was more relaxed. This might have happened
as a consequence of species impoverishment, a feature usually observed
on islands where the insular communities typically show an expanded niche
width compared to their mainland counterparts (MacArthur et al., 1972).
Terrestrial examples of succession following glacier retreat in the Antarctic
showed a general increase in diversity of plants, mites and nematodes with
time as the soil was deglaciated (Ileva-Makulec and Gryziac, 2009; Gryziac
2009; Favero-Longo et al., 2012), and a dependence of secondary
colonization by metazoans on the primary colonization of lichens and
bryophytes (Gryziac 2009). At both Faro and Isla D, as a consequence of
the glacier retreat, new substrate became available for colonization by
macroalgae (Quartino et al., 2013). Further, we recently observed that at
Isla D there was a high occurrence (~40% of surface sediment microalgae)
of sea-ice and phytoplanktonic algae (sampling of February 2010, Pasotti et
al., 2014b). We observed that both indicators of isotopic niche width (SEAc
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Chapter III. Trophic interactions
and SEAb) were larger for Isla D and to a lesser extent also in Faro,
compared to Creek. The additional resource pool represented by these
primary producers could be an explanation for the wider isotopic niche
(wider primary producers isotopic niche) of the local assemblages found at
these two sites (e.g. more exploitable resources available, more trophic
niches available) compared to the station influenced by the meltwater
stream. As well, the younger age of the Isla D site in regards to its ice-free
status and the occurrence of ice-scour events would have resulted in more
trophic niches available at various moments during the past few years. At
Creek station on the other hand, the longer ice-free history of the site may
have been long enough to allow the benthos to develop into a more
established (despite the ongoing disturbances) and efficient food web
(smaller SEAs, Abrantes et al., 2014), maximizing the exploitation of the
available resources.
Additionally Isla D is characterized by a high sedimentation and
intermediate ice disturbance (Quartino et al., 2013; Pasotti et al., 2014b),
but yet it appears to be a low energy environment where wave action is less
important (Wölfl et al., 2014). Pasotti et al. (2014b) identified the relative
high dominance of the nematode genus Microlaimus and the higher
abundance of harpacticoid copepods at the Isla D site. Microlaimus is
known to be a successful colonizer of fresh ice-scoured sediments (Lee et
al., 2001b) and to be present in intermediate/late stages of succession after
the collapse of the Larsen B ice shelf (Raes et al., 2009). Seemingly,
harpacticoid copepods have been reported as fast colonisers of scoured
(Lee et al., 2001b) and artificial bare (Veit-Köhler et al., 2008b) sediments.
The very elongated shape of the SEAc ellipse at Isla D, was mainly due to
the meiofauna size class assemblage. Within this size group, the epibiosis
trophic strategy identified in the meiobenthic harpacticoid copepod (MT2)
was present only at this site. This morphotype stable isotope analysis
showed negative δ15N and very depleted δ13C values. At Isla D, also
cumaceans were found to carry epibiont ciliates on their exoskeleton (F.
Pasotti, pers. observ.). This strategy was not observed in the other two sites
during our sampling effort. Nevertheless, as previously explained in the
results, the larger SEAc and SEAb of Isla D were not due to the presence of
this single life strategy, but it seems that isotopic niche distribution was
wider at the site in light of the overall meiobenthic isotopic niche width. It
seems that thanks to their specific functional traits, meiobenthic organisms
can respond to high ice disturbance and the newly available resource pool
via fast colonization processes and by establishing more differentiated
trophic niches during the first years after these events.
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Chapter III. Trophic interactions
The benthos at Faro benefited (e.g. higher overall biomasses, Pasotti et al.,
2014b) from the lower frequency of ice-scouring events (Phillip et al. 2011),
although it was subject to important wave activity (Wőlfl et al., 2014). The
resulting sediment re-suspension could, however, sustain the abundant
filter and suspension feeders community found there (Pasotti et al., 2014b).
A strong benthic-pelagic coupling sustaining a detritus-based sediment
community where macrofauna remineralised detritus (e.g. faecal pellets)
was suggested to explain the available food for the meiobenthic deposit
feeders, although from our results (see δ13C values Fig. 3) MPB seems to be
an important food source for the meiofauna. At Faro the SEAc showed
indeed an intermediate position and a compacted shape, with relatively
higher trophic levels (δ15N values) of meiofauna taxa. This may be indicative
that the macrobenthos relies on a mixture of food sources and meiofauna
may be composed of organisms with likely predatory feeding habits.
Creek site is affected by intermediate levels of inorganic sedimentation, by
sediment re-suspension and by rather high ice disturbance (Pasotti et al.,
2014b; Philipp et al., 2011; Wölfl et al., 2014). Rocky substrate is completely
absent and hence fresh macroalgae detritus is likely to be less abundant in
these sediments but it can be transported via the currents from other
locations. The macrobenthic biomass dominated the site, with the
scavenger polychaete Barrukia cristata being the most conspicuous
species (Pasotti et al., 2014b). The meiofauna was lower in abundance but
the nematode community was well adapted to the local conditions showing
a higher evenness among genera (Pasotti et al., 2014b). From our present
study, the isotopic niche width at Creek site was the smallest and showed
the highest relative position in the bi-plot space. The high degree of
disturbance resulting from the glacial meltwater stream and the likely
frequent re-suspension and ice-scouring events may force the community
to a more efficient use of the available resources which are finally
transferred to the higher trophic levels. Not surprisingly, SEA c ellipse of
Creek community overlapped for 80% with that of Faro, suggesting a
possibly similar “centralized” isotopic niche with a short food chain and an
efficient resource use.
Spatial patterns: redundancy
When species with different life strategies colonize a ‘new’ environment the
functional diversity increases locally, and so the trophic niche is expected
to widen. With time an increase in trophic redundancy can be expected,
since newcomers often share similar functional traits, as already observed
for stream communities after glacial retreat in southeast Alaska (Brown and
Milner, 2012). The analysis of the mean nearest neighbor distance (MNND)
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Chapter III. Trophic interactions
and its standard deviation (SDMNND) can give some indications on the
trophic redundancy found at the three sites. The first metric is a measure of
the species packing (in the bi-plot space), but it is more dependent on
sample size. The second, is a measure of the evenness of species trophic
niche distribution, and it is less influenced by sample size. Our analysis
showed that the three assemblages did not display significant differences in
trophic redundancy, although MNND was always slightly higher at Isla D
compared to the two other stations (e.g. lower species packing or lower
trophic redundancy) and Creek showed a slightly higher SDMNND than the
other two sites (e.g. less even distribution of trophic niches or lower trophic
redundancy). Isla D and Creek are the sites that experience the higher
levels of ice-disturbance and which showed the most patchiness in the
community distribution (Pasotti et al., 2014b). However, the Bayesian
probabilities for these differences can be questioned (they were never
higher than 60 %, see Addendum Table A6) and a lack of differences in
redundancy seems the most logical outcome. The sites were already icefree for several years at the time of sampling (at least eight years for Isla D),
and because of their small distance and the local cyclonic current system
(Roese and Drabble, 1998; Schloss et al., 2012), the communities may have
shared already most of the species/taxa (and hence, most of the trophic
diversity). Finally, the very high degree of omnivory that appears to
characterize Potter Cove benthos’ trophic network (see before) and the fact
that what our observations cannot be considered indicative of a primary
colonization, may hamper the utility of these metrics to detect the
colonization direction in this shallow water environment.
Size by site comparison: trophic niche width
A “size by site” comparison of the SEAc ellipses (Fig. 7), showed specific
patterns for the different site. The meiofauna ellipse was wider at Isla D and
it encompassed the isotopic niche ellipses of the two macrofauna size
classes. At Isla D site a continuous intermediate level of ice-scour
disturbance appears and re-colonisation can be locally stimulated. Most of
the macrofauna biomass was made up by mobile scavengers and
predators and was relatively low compared to the other two sites (Pasotti et
al., 2014b), whereas the meiofauna showed to be numerous and
comparable in biomass to the other investigated locations. Meiofauna taxa
are known to be rapid colonizers after ice-scour re-colonisation (Lee et al.,
2001b) and to be less sensitive to sediment mechanical instability than
macrofauna (Warwick et al., 1990).
At Faro the SEAc of meiobenthic organisms is positioned on top of the two
macrobenthos ellipses. This seems to point to the fact that the meiofauna
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Chapter III. Trophic interactions
relies on macrobenthic-derived detritus for its diet. Pasotti et al. (2014b)
already suggested that the benthic-pelagic coupling at this site seem to be
strong. Tatián et al., (2008a) also suggested that the faecal pellets of filter
(and suspension) feeders could be an important source of organic matter
for the surrounding sediments.
Creek benthos did not show any clear pattern in relation to the size class
ellipses. The food chain looks more compact, and the recycling of the
locally available organic matter could likely be efficient. This can be due to
the high level of sediment re-suspension (Wölfl et al., 2014) and remixing.
Moreover the food web seems to be dominated by deposit feeders,
scavengers and predators, like at Isla D, and this is linked to the high icescour disturbance and related higher mortality found at this site (Pasotti et
al., 2014b). The high incidence of ice-scour can produce a high amount of
dead animal material on the sediment, and the likely recycling and
reutilization of this organic matter may justify the high position of the ellipses
in the bi-plot space.
Reduced dataset analysis: highlights
When running the analysis without the harpacticoid copepod MT2 and the
two polychaete species in Isla D, we found an important influence of these
samples on the overall inter-site comparison results (see tables in the
Addendum A4 - A6 for resume). The posteriori Bayesian probability pointed
now to an inverted order in the SEAs with Faro showing the larger area,
followed by Creek and Isla D. Moreover excluding the epibiosis life strategy
from the analysis and hence from the meiofauna size class, the overall by
size comparison (see Addendum Fig. A3) analysis showed significant
differences from the complete dataset analysis, with increasing trophic
niche width at increasing size spectra (Bigger macrofauna > Smaller
macrofauna > Meiofauna). When looking at the size by site situation, at Isla
D the bigger macrofauna SEAc now showed very reduced trophic niches,
and the meiobenthos occupied the highest position compared to the other
two size classes. Isla D bigger macrofauna appeared to exploit mostly the
basal resources (lower δ15N) lacking the higher TLs. Moreover, the size
spectra ellipses (or isotopic niches, see Fig. A3) show a clear separation at
the most newly ice-free site compared to those of Creek and Faro. The
removal of the copepod MT2 and of the higer TLs of the bigger macrofauna
from the Isla D dataset, resulted in more centered ellipses with a lower
dispersion of the data points. This is statistically confirmed by the
observation of the Layman’s metrics and Bayesian statistic for the three
sites comparison (See table A6). Now Isla D shows the larger values for all
the metrics compared to the Creek and Faro, with a minimum Bayesian
105
Chapter III. Trophic interactions
posterior probability of >80%. This result is logical seen that by reducing
the simulated ranges at Isla D (by taking away the “outliers”) the mean
became higher. Interesting enough, from the observation of the MNND
metric (a measure for the overall density of species packing, Layman et al.,
2007), we observe a significantly higher value - and hence lower trophic
redundancy - at Isla D. This would corroborate the interpretations arising
from the complete dataset analysis, where the larger SEAb and SEAc at Isla
D led us to the conclusion that the longer – hypothethical - isolation of the
site and the repeated colonization processes - due to ice scouring - would
allow more life strategies to settle (MacArthur et al., 1972). By eliminating
only a few of these life strategies from the analysis highlighted the
importance of the (recent) age in terms of ice-free state (the lesser the time
a site had experienced colonization, the lower the redundancy in trophic
functions that can be expected, Brown and Milner, 2012) in the overall
interpretation of the metrics and SEAs from the new analysis. Lastly, from
the reduced dataset analysis the higher trophic diversity (SEAs) are
observed where the level of disturbance (e.g. ice scouring and inorganic
sedimentation) is intermediate to low (Faro), a pattern already observed in
streams (Townsend et al., 1997). The two analyses complement eachother
in providing a wider view of the potential underlying processes that are
shaping the shallow benthic assemblages at these inner sites in Potter
Cove.
4.2. General considerations: functional traits in Potter Cove benthic
food web
Overall, the benthic food web at the three Potter Cove contrasting sites
showed the presence of several levels of consumers spanning from the
wide stable isotopes range of deposit feeders (De/O) to the more defined
range of predators (Pr/O) and scavengers (Sc/O), as it was also registered
for an integrated food web analysis of the whole Potter Cove system in a
complementary study by Tarantelli et al. (in prep.). We identified a total of
four consumer trophic levels (TLs) by means of a reduced (Δδ15N = 1.8‰)
invertebrate/plant based-diet fractionation step (McCutchan et al., 2003)
and which resulted in an over-fractionated (1 extra consumer TL) food web
if compared to the standard application of a constant higher-protein based
diet fractionation step of Δδ15N of 3‰ (which lead in fact to a total of three
consumerTLs). With this double approach we wanted to stress and highlight
the potential effects of diet type and omnivory on total food web length. The
benthis organisms under study are mostly feeding on other invertebrate
organisms (e.g. by scavenging, predation or unspecific injestion of
sediment) or on various types of detritus (e.g. by selective or non-selective
deposit feeding) which may be of both algal (fresh or dead micro106
Chapter III. Trophic interactions
/macroalgae) or invetebrate-derived (e.g. faecal pellets, reworked
invertebrate carcasses) origin. This generalist feeding behaviour adds more
levels of recycling within the food web, in a sort of “trophic continuum”. This
could eventually hyde (isotopically) the real final trophic role an organism
could effectively cover (e.g. many polychaetes can be predators on smaller
invertebrates but as well feed unselectively on microalgae) therefore
shortening the total food chain length. This “trophic continuum” can be also
reflected in the width of the stable isotopic signature of the De/O consumer
group and in the overlap of the various consumer categories, showing how
difficult it is to segregate the trophic categories based on their nitrogen
isotopic signatures. It suggests that we may have more feeding plasticity
than estimated and trophic fractionation would need to be fitted to the
actual diet of the organisms.
The food web in Potter Cove has long be suggested to very likely relying on
macroalgae detritus (Quartino et al., 2013) in view of the locally high benthic
biomasses and the usually low local phytoplankton production (Schloss et
al., 2012). Macroalgae detritus (small leave fragments) was found to be part
of the diet of filter and suspension feeder key species in Potter Cove (Tatián
et al., 2004, 2008b) and many grazer amphipods can feed directly on this
algal resource pool. It is important to mention that different macroalgae
species can have very different palatabilities for their direct consumers, for
several species among the most abundant macroalgae groups produce
chemical defenses that repell their grazers (Amsler et al., 2005). Among
Antarctic seaweeds the most palatable species is thought to be Palmaria
decipiens, which unfortunately wasn’t accessible during our sampling,
although present in the cove. Since macroalgae biomass is mostly thought
to be important for the detrital food web (Amsler et al., 2005; Quartino and
Boraso de Zaixso, 2007) we decided to pool the investigated macroalgae
species together and work during our analysis with an average trophic
range for this detrital food source. Another algal potential food source, the
microphytobenthos (MPB), has not yet been quantified in the cove, but its
importance as food for the benthos has been suggested by other authors
for the adjacent Admirality Bay benthos (Corbisier et al., 2004). In this
investigation macroalgae presented a wide range of δ13C values,
overlapping with the sediment carbon signatures, but presenting a rather
depleted signal. On the other hand, the majority of the organisms displayed
intermediate to enriched δ13C values, likely pointing to the importance of
fresh summer microphytobenthos for the cove food web. In fact the MPB
signal was the most enriched among the investigated food sources. For
instance, the baseline organism Yoldia eightsi shows a rather clear MPB
signal, since its carbon values are slightly more enriched (by 1.35‰) than
that of the microalgae. Nevertheless, our interpretations may suffer of small
107
Chapter III. Trophic interactions
limitations: i) the MPB was sampled only from the vicinity of Faro; ii) other
food sources (e.g. sea ice algae) important for the benthic organisms are
missing in our sampling effort since released from the ice in spring. When
looking in detail to the most important meiobenthic group, the nematodes,
we can see a strong link to the local signature of sediment (Fig. 3 and Table
1). Nematodes assemblages are generally dominated by non-selective
deposit feeder taxa (Pasotti et al., 2014b), and the intermediate value we
found in this work lies between their site-specific sediment value and the
MPB value, confirming some feeding plasticity at the community level.
Finally, the very depleted δ15N values of some filter feeder species may
point to a higher contribution of SPM to the diet of these organisms rather
than to a contribution of phytoplankton. The SPM helps as well to explain
the rather large width we identified for the first consumers trophic level (TL1)
when considered the water column and the sediment as one benthicpelagic trophic environment. Nevertheless it is important to stress that the
sampling method for the phytoplankton collection we used in this work may
have missed to sample those components smaller than 55 µm (the lower
limit of our mesh size) and hence fail to find possible trophic connections
between smaller phytoplankton and the investigated filter feeders.
Bacterial degradation may affect carbon and nitrogen stable isotope
organic matter signatures (Lehmann et al., 2002), often either significantly
increasing or decreasing the δ15N values. Organic matter recycling may
have an important role in the cove’s sediments thanks to the abundant
bacterial community (Pasotti et al., 2014b). The tighter connection that the
meiobenthos has with the “small food web” of microrganisms may be one of
the reasons behing the generally high δ15N values of these small metazoan
taxa (see Fig. 2 and 7). Reworked organic matter and other type of detritus
(e.g. filter feeders faecal pellets, Tátian et al., 2008b) can enter the higher
trophic levels of the benthic system via deposit feeding, or else, be
available to benthic suspension feeders via the frequent re-suspension
events during the summer months. Taken this into account, omnivory
(feeding plasticity with potential to feed on both microalgae, macroalgae
and bacteria) and deposit feeding (feeding on unselected sediment organic
matter) appear to be ideal strategies in this shallow water polar system.
There are a few studies which found that the capacity of Antarctic
metazoans to shift between food sources (Dunton, 2001; Kaehler et al.,
2000; Pasotti et al., 2012; Tatián et al., 2004, 2008b) may be linked to the
strong seasonality in fresh primary production (Dayton et al., 1994; Peck et
al., 2005; Tatián et al., 2004). Since Antarctic shallow water and deeper
shelf sediments seem to be virtually never deprived of food during austral
winter as shown by the continuously high benthic standing stocks in many
108
Chapter III. Trophic interactions
coastal and shelf areas, organisms appear to cope with the strong
seasonality in fresh food input (Barnes and Clarke, 1994; Pasotti et al.,
2014a; Smith et al., 2006; Vanhove et al., 2000). Nevertheless, the
palatability of the available winter organic matter has been questioned
(Pasotti et al., 2014a) and the inter-annual variability in local primary
production may be the reason for animal’s diet flexibility (Smith et al., 2006,
2008). Re-suspension events in summer are an important environmental
feature in the shallow waters of Potter Cove (Wölfl et al., 2014). This can
explain the non-selectivity of filter and suspension feeders (Tátian et al.,
2004). Indeed, in a parallel study (Tarantelli et al., in prep .) we report that
the food web structure of Potter Cove can be better represented by a
“trophic continuum” than by clear separated feeding strategies groups.
Such plasticity would be reflected in a wider trophic niche in these species.
The expansion of trophic niches has been already reported as a possible
response to physical or chemical stressors in freshwater snails (Bayona et
al., 2014) and terrestrial insects (Colas et al., 2014). Antarctic marine
ecosystems are known as extreme environments and the unique physical
characteristics of these biomes can be considered as possible stress
factors for the inhabiting organisms. Thus omnivory can be considered as
an evolutionary strategy of Antarctic metazoans to lower their stress while
coping with their challenging environment.
5.
Acknowledgments
We acknowledge the vERSO project (www.versoproject.be, funded by the
Belgian Science Policy Office (BELSPO, contract n°BR/132/A1/vERSO) and
the EU project Imconet (FP7 IRSES, action no. 319718) for financial and
networking support. We would like to thank all the military and scientific staff
at Carlini base for their valuable assistance during the sampling process. A
special thank goes to Óscar Gonzáles and Doris Abele for their logistic
support.
109
Chapter III. Trophic interactions
Table 1 Stable isotopes values (average ± standard deviation) of food sources and consumers. N(R) = number of individuals (per
number of replicas); Bayesian modeling grouping = size class grouping used in the SIBER program. Where applicable taxa have
the specification of the site: Creek (C), Faro (F), Isla D (I).The sign “ means that the reference is the same as above.
Taxon
Algae
Macroalgae
Microphytobenthos
Phytoplankton
Sediment POM
Cnidaria
Pennatulacea
Tunicata
Ascidiacea
Ectoprocta
Crustacea
Mysida
N(R)
δ13C
δ15N
Bayesian size
grouping
Trophic group
References for trophic group
Suspended Particulate Matter s
22
-26.08 ± 1.17
0.45 ± 1.17
NA
SPM
Macroalgae
Microphytobenthos
200 µm mesh
50 µm mesh
Sediment (Faro) 0-5 cm
Sediment (Faro) 0-1 cm
Sediment (Isla D) 0-5 cm
Sediment (Isla D) 0-1 cm
Sediment (Creek) 0-5 cm
Sediment (Creek) 0-1 cm
22
1(2)
(5)
(3)
10(2)
1(2)
10
1(2)
10
1(2)
-25.03 ± 5.45
-13.15 ± 0.35
-25.31 ± 1.47
-23,41 ± 0.85
-20.81 ± 1.21
-18.72 ± 0.56
-18.84 ± 1.8
-17.84 ± 1.06
-22.54 ± 1.09
-21.53 ± 1.6
3.08 ± 0.85
4.90 ± 0.14
4.33 ± 0.54
4.69 ± 0.34
3.26 ± 0.77
3.35 ± 0.19
3.25 ± 0.89
3.86 ± 0.67
4.01 ± 0.68
4.55 ± 1.00
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
Macroalgae
MPB
Phytoplankton 200 µm
Phytoplankton 55 µm
Sediment
Sediment
Sediment
Sediment
Sediment
Sediment
Malacobelemnon daytoni (F)
1(3)
-22.64 ± 0.3
7.14 ± 0.22
Bigger Macrofauna
Filter/suspension feeder
Kozloff, E. N. 1990; Best 1988
Molgula pedunculata (I)
Corella eumyota (I)
Cnemidocarpa verrucosa (I)
Bryozoan (I)
1(2)
1(3)
1(2)
1
-23.57 ± 0.01
-23.99 ± 0.1
-24.24 ± 0.23
-25.48
4.69 ± 0.00
4.58 ± 0.08
5.83 ± 0.67
3.52
Bigger Macrofauna
Bigger Macrofauna
Bigger Macrofauna
Bigger Macrofauna
Filter/suspension feeder
Filter/suspension feeder
Filter/suspension feeder
Filter/suspension feeder
Tátian et al., 2008a,b
“
“
Ruppert & Barnes, 1994
Mysid
1
-21.36
6.10
NA
Zooplankton
Wittmann, 1996; Ruppert &
Barnes, 1994
110
Chapter III. Trophic interactions
Table 1. Continued
Taxon
Tanaidacea
Nototanaid MT1 (F)
N(R)
δ13C
7(2)
-20.92 ± 1.96
δ15N
4.90 ± 0.66
Bayesian size grouping
Smaller Macrofauna
Trophic group
deposit feeder/omnivore
References for
trophic group
BlazewiczPaszkowyczi and
Ligowski, 2002
Nototanaid MT2 (F)
8(3)
-15.48 ± 0.86
4.80 ± 0.20
Smaller Macrofauna
deposit feeder/omnivore
“
Cumacea
Eudorella sp. (F)
Eudorella sp. (I)
Eudorella sp. (C)
Dyastilis sp. (I)
Eudorella sp. (F)
Eudorella sp. (C)
Calanoids copepods
-17.05 ± 0.07
-16.45 ± 1.06
-19.45 ± 0.84
-21.8 ± 0.14
-16.63 ± 0.01
-14.07
-24.19 ± 1.1
7.65 ± 0.07
7.05 ± 0.21
7.05 ± 0.21
5.70 ± 0.00
13.75 ± 0.6
10.07
6.77 ± 0.38
Smaller Macrofauna
Smaller Macrofauna
Smaller Macrofauna
Smaller Macrofauna
Meiofauna
Meiofauna
NA
deposit feeder/omnivore
deposit feeder/omnivore
deposit feeder/omnivore
deposit feeder/omnivore
deposit feeder/omnivore
deposit feeder/omnivore
Zooplankton
“
“
“
“
“
“
Copepoda
5(2)
5(2)
5(2)
5(2)
8(2)
8(1)
3(7)
Harpacticoids MT2 (I)
40(1)
-34.9
-2.6
Meiofauna
bearing ectosymbiont
deposit feeder/omnivore
Harpacticoids MT1 (I)
40(1)
-20.05
10.34
Meiofauna
Isopoda
Paraserolis polita (F)
1(2)
-16.65 ± 1.06
12.1 ± 0.56
Bigger Macrofauna
predator/omnivore
Amphipoda
Phoxocephalidae (C)
3(5)
-16.2 ± 0.31
11.33 ± 0.27
Smaller Macrofauna
scavenger/omnivore
Phoxocephalidae (F)
3(2)
-14.38 ± 0.75
7.83 ± 0.04
Smaller Macrofauna
scavenger/omnivore
Amphipod MT1 (F)
Amphipodes (I)
1(3)
5(2)
-17.61 ± 0.00
-19.71 ± 1.60
10.59 ± 0.01
8.99 ± 0.70
Smaller Macrofauna
Meiofauna
scavenger/omnivore
scavenger/omnivore
Yoldia eightsi (F)
1(3)
-11.81 ± 0.84
8.75 ± 0.42
Bigger Macrofauna
deposit feeder/omnivore
Mollusca
Bivalvia
Yoldia eightsi (C)
1(3)
-11.76 ± 0.81
8.12 ± 0.27
Bigger Macrofauna
deposit feeder/omnivore
Walkusz and
Rolbiecki, 2007
De Troch et al., 2005;
Ustach, 1982
Bick and Arlt, 2013
Guerra-garcía et al.,
2014; Nyssen, 2005
Guerra-garcía et al.,
2014; Nyssen, 2005
Nyssen 2005
“
Davenport, 1988
“
111
Chapter III. Trophic interactions
Table 1. Continued
N(R)
δ13C ± SD
δ15N ± SD
Bayesian size grouping
Trophic group
Nematodes (F)
600(1)
-17.99
8.60
Meiofauna
deposit feeder/omnivore
Taxon
Nematoda
References for trophic group
Jensen, 1987; Pasotti et al.,
2012
“
“
Nematodes (I)
600(1)
-16.5
8.25
Meiofauna
deposit feeder/omnivore
Nematodes (C)
600(1)
-18.5
10.10
Meiofauna
deposit feeder/omnivore
Nephtydae
Aglaophamus trissophyllus (C+I)
1(3)
-14.27 ± 0.08
12.58 ± 0.07
Bigger Macrofauna
predator/omnivore
Fauchald and Jumars 1979
Polynoidae
Barrukia cristata (C+I)
1(3)
-16.96 ± 0.17
11.74 ± 0.06
Bigger Macrofauna
predator/omnivore
Corbisier et al., 2004b;
Fauchald and Jumars 1979
Polychaeta
Cerratulidae (F)
-18.06 ± 0.45
8.35 ± 0.30
Smaller Macrofauna
deposit feeder/omnivore
Fauchald and Jumars 1979
-14.12 ± 0.5
-18.27 ± 0.27
7.69 ± 0.18
8.64 ± 0.34
Smaller Macrofauna
Smaller Macrofauna
deposit feeder/omnivore
deposit feeder/omnivore
“
“
Opheliidae (F)
5(3)
1(2)
10(2)
-19.35 ± 0.42
11.52 ± 1.42
Smaller Macrofauna
deposit feeder/omnivore
“
Capitellidae (F)
10(1)
-15.49
12.62
Smaller Macrofauna
deposit feeder/omnivore
“
Capitellidae (C)
5(2)
-17.09 ± 0.58
9.85 ± 0.46
Smaller Macrofauna
deposit feeder/omnivore
“
Maldanidae MT1 (F)
Maldanidae MT2 (F)
Capitellidae (F)
Cirratulidae MT1 (C)
Cirratulidae MT2 (C)
Orbiniidae (F)
Cirratulidae (F)
1(3)
1(3)
5(3)
5(3)
10(1)
5(3)
5(3)
-15.89 ± 0.06
-19.68 ± 0.14
-19.01 ± 0.10
-18.30 ± 0.03
-18.15 ± 0.57
-19.34 ± 0.42
-18.28 ± 0.03
10.34 ± 0.7
9.64 ± 0.35
12.49 ± 0.3
7.58 ± 0.04
12.36 ± 0.54
11.51 ± 1.41
11.26 ± 0.24
Smaller Macrofauna
Smaller Macrofauna
Meiofauna
Meiofauna
Meiofauna
Meiofauna
Meiofauna
deposit feeder/omnivore
deposit feeder/omnivore
deposit feeder/omnivore
deposit feeder/omnivore
deposit feeder/omnivore
deposit feeder/omnivore
deposit feeder/omnivore
“
“
“
“
“
“
“
Ampharetidae (I)
1(1)
-15.90 ± 0.84
8.1 ± 1.14
Smaller Macrofauna
deposit feeder/omnivore
Fauchald and Jumars 1979
predator/omnivore
Shirley and Morris, 1990; Trott,
1998
Cerratulidae (C)
Spionidae (F)
Priapulida
5(6)
Priapulus sp.(F)
1(3)
-17.99 ± 0.44
10.7 ± 0.49
Smaller Macrofauna
112
Chapter IV. Temporal analysis
Remaining of a boulder as testimony of glacier retreat and the joint
weathering action of water and freezing
"We must always remember with gratitude and admiration the first sailors
who steered their vessels through storms and mists, and increased our
knowledge of the lands of ice in the South."
Roald Amudsen
Antarctic explorer
(1872-1928)
Chapter IV. Temporal analysis
Adapted from:
Pasotti, F., Convey, P. and Vanreusel, A.: Potter Cove (west Antarctic
Peninsula) shallow water meiofauna: a seasonal snapshot, Ant. Sci., 10, 110, 2014.
Abstract
The meiobenthic community of Potter Cove (King George Island, West
Antarctic Peninsula) was investigated, focusing on responses to
summer/winter conditions in two study sites contrasting in terms of organic
matter inputs. Meiofaunal densities were found to be higher in summer and
lower in winter, although this result was not significantly related to the in situ
availability of organic matter in each season. The combination of food
quality and competition for food amongst higher trophic levels may have
played a role in determining the standing stocks at the two sites.
Meiobenthic winter abundances were sufficiently high to infer that energy
sources were not limiting during winter, supporting observations from other
studies for both shallow water and continental shelf Antarctic ecosystems.
Recruitment within meiofaunal communities was coupled to the local
seasonal dynamics for harpacticoid copepods but not for nematodes,
suggesting that species-specific life history or trophic features form an
important element of the responses observed.
Keywords: Meiofauna, benthos, seasonality, standing stocks, shallow
waters, west Antarctic Peninsula
1.
Introduction
The Antarctic marine ecosystem, with its cool water temperatures and
strong seasonal fluctuations, represents a unique environment. During the
austral summer light is available to primary producers such as microalgae
(phytoplankton, sea-ice algae and microphytobenthos) and macroalgae,
which are responsible for fixing much of the carbon utilized by marine
organisms (Thomas et al., 2008). In spite of the obvious seasonality one of
the early paradigms, that “the Antarctic sessile benthos subsists trophically
on the strong seasonal input of phytoplankton blooms and ceases feeding
during the remainder of the year”, has subsequently been subject to
challenge and re-evaluation (e.g. Arntz and Gili, 2001; Clarke, 1988).
Several recent studies carried out both on the deeper continental shelf and
in shallow water coastal sediments (Bowden, 2005; Echeverría and Paiva,
2006; Smith et al., 2012) have demonstrated no cessation in feeding in
winter and the presence of a “food bank”. This, coupled with the previously
113
Chapter IV. Temporal analysis
unrecognised capacity of at least some organisms to feed on different
elements of the plankton (e.g. protists, nano- and picoplankton via detritus
re-suspension) allows constant macrobenthic standing stock and
community composition, and possibly even year-round recruitment (Arntz &
Gili 2001).
Most research in this field to date has focused on the benthic macrofauna,
and the meiofauna has been only poorly investigated, despite its
importance for organic matter remineralization and nutrient cycling, and its
role as food for higher trophic levels. Until now only Vanhove et al. (2000), in
a study carried out at Signy Island (South Orkney Islands) have addressed
the possible relationship between meiofaunal standing stock and primary
production, based on fortnightly sampling over one year in a shallow site.
Other studies have linked shallow Antarctic meiofaunal taxa abundances
and distribution to sediment grain size and/or spatial variation in organic
matter input (Hong et al., 2011; de Skowronski & Corbisier, 2002; VeitKöhler, 2005; Veit-Köhler et al., 2008a). Pasotti et al. (2012) performed
laboratory tracer experiments to compare the importance of bacteria versus
microalgae for a number of Antarctic meiofaunal taxa. Their results showed
that different meiobenthic groups had different feeding capacities for the
two labelled food sources used. However the overall carbon uptake was too
low to provide their putative metabolic requirements, leading to the
conclusion that other food sources were relevant for these meiobenthic
metazoans. Tightly linked to the sediment they inhabit, most meiofauna lack
pelagic larvae (Palmer 1988) and it is therefore likely that recruitment will be
linked to food availability and local biogeochemical conditions.
The present study focused on advancing understanding of the seasonal
differences in Antarctic meiofauna, comparing two adjacent shallow water
sites contrasting in terms of sediment characteristics, food availability in
winter, and their location and surroundings. We addressed the hypotheses
that: 1) meiofaunal density and nematode biomass are higher in summer
compared to winter due to the greater availability of freshly-produced
organic material; 2) the main meiofaunal taxa (copepods, nematodes)
recruit during the summer season; 3) the most abundant taxa show similar
responses in terms of abundance, biomass and juvenile/adult ratio.
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Chapter IV. Temporal analysis
2.
Materials and methods
2.1. Study site and sampling strategy
Two sites were selected in Potter Cove (PC), a fjord-like embayment on the
southern coast of King George Island (Isla 25 de Mayo; South Shetland
Islands) situated to the north-west of the Antarctic Peninsula (Fig. 1). The
bay is characterized by the presence of a retreating glacier and relatively
shallow depths, with a maximum depth of about 50 m. A clock-wise
circulation brings sediment-free waters from Maxwell Bay into the cove
(Klöser et al., 1994; Schloss and Ferreyra, 2002; Schloss et al., 2002).
Fig. 1. Map of King George Island location and Potter Cove, showing the two study
sites (ST1, ST2).
The study sites were two shallow water (15 m depth) stations, located on
the opposing shores of the cove (Fig. 1). Station 1 (ST1) was adjacent to the
Potter Peninsula (62°14'07.2''S, 58°39'56.2''W), a few hundred meters from
the outflow of Potter Creek, a river that flows during the summer months and
carries high loads of land-derived material. Station 2 (ST2) was on the north
shore, adjacent to the Barton Peninsula, where it is mainly influenced by the
clear waters entering the cove.
115
Chapter IV. Temporal analysis
At the two sites, in late November 2009 (early summer samples) and midAugust 2010 (winter samples), sediment samples were taken by scuba
diving using perspex push cores (5.4 cm inner diameter, 22.89 cm 2 surface
area, 10-14 cm sediment depth). At each station and sampling occasion a
total of six replicate sediment cores were obtained: three in order to make
meiofaunal community analyses, and three for pigment, total organic
carbon (TOC), total nitrogen (TN) and grain size analyses. The top two
centimetres (0-2 cm) were carefully cut from the core. For meiofaunal
community analysis these were stored in formaldehyde (4%, buffered with
sea water), whilst for pigment and grain size analyses the samples were
kept frozen (-20°C) in the dark until processing. The 0-2 cm layer was
selected since previous studies in PC have confirmed that it contains the
majority of taxa (e.g. in the 2-5 cm layer virtually only nematodes and
polychaetes) and contributes more than 50% of the total meiofauna
community of the 0-5 cm layer (Pasotti et al., 2012). Temperature and
salinity at 15 m depth in the inner cove in January 2010 was around + 0.9°C
and 34.07 PSU respectively (Hernando Marcelo, Universidad del Mar del
Plata, pers. comm.).
2.2. Environmental variables
Grain size analysis was carried out on the three replicates using a Malvern
Mastersizer 2000 analyzer, after sieving the coarse fraction (boulders,
pebbles) on a 1000 mm screen. Sediment fractions from 0.4 to 900 mm
were expressed as volume percentages and classified according to the
(Wentworth, 1922) system. After testing for significant differences with
Permanova and running a draftsman plot on the detailed size classes (<4
µm, 4 - 63 µm, 63 - 125 µm, 125-250 µm, 250 -500 µm, >500 µm; data not
shown), we identified considerable redundancy between some of them. In
light of the high redundancy of the various sediment size classes and in
order to generate a readable output from the PCA analysis we carried out
on the complete set of environmental variables, we decided to group the
sediment size classes into two classes, namely silt (0.4-63 µm) and sand
(63-1600 µm). For this reason both the Permanova results and the PCA
analysis showed in this study only report results of analysis that include
these two size classes.
Total sedimentary nitrogen (TN), total organic carbon (TOC), total carbon
(non-acidified samples) to nitrogen ratio (C/N) and organic carbon
(acidified samples) to nitrogen (Corg/N), were determined on triplicate dried
and, when needed, acidified (with 10 N HCl) sediment samples using a
Flash 2000 Organic Element Analyzer.
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Chapter IV. Temporal analysis
Pigment concentration analysis was carried out on three replicates obtained
at each site and sampling occasion. The sediment was first lyophilized and
homogenised, then extracted in 90% acetone, separated using reversephase HPLC, and, finally, the resulting solution was subjected to
spectrophotometric analsysis with a fluorescence detector (Gilson Inc.,
model number 121) in order to estimate the pigment concentration (Jeffrey
et al., 1997). Chloroplast Pigment Equivalents (CPE, µg g-1 dry sediment)
were derived as the sum of chlorophyll a (chl-a) and its degradation
products (phaeopigments). Fucoxanthin concentration (µg g-1 dry weight
sediment) was used as an indicator of brown/golden brown algae presence
(Dring, 1982). Values are reported as mean ± standard deviation (SD).
2.3. Meiofaunal abundance and biomass
The extraction of meiofauna followed standard procedures of
centrifugation–rotation with LUDOX HS40, and sieving over 1000 and 32 µm
sieves (Heip et al., 1985; Vincx, 1996). Counting was carried out following
sub-replication with a meiofauna sample splitter (Jensen, 1982) for the more
numerous taxa (nematodes, copepods and their naupliar larvae), with total
counts being completed for other taxa. From the sample splitter, which
contains a total of eight chambers, we randomly selected three to be used
as sub-replicates of the sample, for the counting of nematodes, copepods
and nauplii. Nematodes were identified at the genus level, collecting about
100 individuals randomly from each replicate and mounting them on glass
slides. The online identification key for free-living marine nematodes
(NeMysKey©) developed within Nemys (http://nemys.ugent.be/), and the
key of Warwick et al. (1998) were used. Nematode trophic guild
composition was described based on the definitions given by Wieser
(1953). Standard methods were used for nematode (about 1200 nematodes
per replicate) biomass determination, based on estimation of body volume
using Andrássy’s formula (Andrássy, 1956): V = L * W2 / 16 * 105, where V is
the volume in nanoliters, L is the length in µm (excluding filiform tails, if
present) and W is maximum width in µm. Body volume was converted to
biomass (µg wet weight 10 cm-2) assuming a specific gravity of 1.13
(Wieser, 1960) and a dry/wet weight (DW/WW) ratio of 0.25. Individual
biomass was then converted to carbon assuming a dry weight/µg C ratio of
0.124 (Jensen, 1984). Community biomass values (µg C 10 cm-2) were
calculated as the product of nematode densities (ind. 10 cm-2) and the
arithmetic mean of individual biomass values.
As a tool for the investigation of seasonality in recruitment dynamics,
juvenile to adult ratio was calculated for nematodes and expressed as the
117
Chapter IV. Temporal analysis
ratio of juveniles versus female and male adults (J/A). For harpacticoid
copepods we calculated the nauplii to copepodids ratio (N/C), where
copepodids included copepodid I – V (juvenile forms) and copepodid VI or
adult forms.
Results values are reported as mean ± standard deviation (SD).
2.4. Statistical analysis
To test for differences between stations and seasons in meiofaunal
densities and biomass (all fauna combined, and analyzing nematodes,
harpacticoid copepods, cumaceans and nauplii separately), nematode
genera, and environmental variables, non-parametric permutational
ANOVAs (Permanova) with a fully crossed three-factor design were
performed with the fixed factor station “st”, next to the fixed factor time “ti”
next to the random factor core “co”. The interaction term “st×ti” gives
information about the differences at each time of the above-mentioned
parameters between the stations.
An Euclidean distance-based resemblance matrix was used for the analysis
of the environmental variables, while a Bray-Curtis similarity resemblance
matrix was used for the abundance and biomass data. In cases of
significant “st×ti” interactions, pairwise tests of “st” and “ti” within “st×ti”
were performed to investigate in which time period (summer or winter) the
stations differed. Because of the restricted number of possible permutations
in pairwise tests, P-values were obtained from Monte Carlo sampling
(Anderson and Robinson, 2003). Permdisp was not used since PERMDISP
analysis for a small sample size with n<5 is not appropriate (Anderson et
al., 2008).
For the nematode genera composition, Multi Dimensional Scaling (MDS)
was performed in order to better visualize the results. Two way crossed
Analysis of Similarity (ANOSIM) was performed in order to test for
differences between stations or times. To represent graphically the
influence of the environmental variables at the different sampling stations a
PCA was run. Abundance and biomass data were fourth root transformed
prior to the analysis of the whole community, while nematode genus relative
abundances were square root transformed. Environmental data were
normalized since variables with different unit measures were analyzed
together.
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Chapter IV. Temporal analysis
Table 1. PERMANOVA results. When the factor “station x time” was not significant,
the pair-wise comparisons (last four columns) were left blank. SUM= summer;
WIN= winter; ns ≥ 0.1.
station
time
station x
time
tot taxa abundances*
0.0406
0.0168
ns
Nematodes
abundances
0.0264
0.0699
ns
Harpacticoids
abundances
0.08
0.0604
ns
Nauplii abundances
ns
0.0368
ns
Cumaceans
abundances
0.01
ns
ns
Nematodes genera*
relative abundances
0.0621
0.0681
ns
Nematodes biomass
ns
0.082
ns
Nematodes individual
biomasses
0.0277
ns
ns
J/A ratio nematodes
ns
ns
ns
N/C ratio harpacticoids
ns
0.0406
ns
Environmental*
0.0385
ns
ns
TOM%
ns
0.08
ns
TOC%
0.0189
ns
0.0124
TN%
ns
ns
ns
C/N
ns
ns
ns
Corg/N
ns
ns
ns
CPE
ns
ns
ns
Fucoxanthin
0.0837
0.0956
ns
Phaeo/Chla
0.0872
0.0702
ns
within level
WIN
"ST1 vs
ST2"
within level
SUM
"ST1 vs
ST2"
within
level
ST1
"SUM vs
WIN"
within
level
ST2
"SUM vs
WIN"
ns
0.0089
ns
0.0134
*= for multivariate analysis
N/C ratio = nauplii to copepods ratio in harpacticoids C/N = carbon to nitrogen ration, TOM%=
total organic matter concentration, TOC%= total organic carbon concentration, TN%= total
nitrogen, C/N = total carbon (non-acidified samples) to nitrogen ratio, Corg/N = organic carbon
(acidified samples) to nitrogen; CPE= chloroplastic pigment equivalents; Phaeo/Chla=
phaeopigments to chlorophyll-a ratio.
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Chapter IV. Temporal analysis
Fig. 2 Principal Component Analysis (PCA) based on the environmental parameters
Chloroplast Pigment Equivalent (CPE), carbon to nitrogen ration (C/N), Fucoxanthin
concentration, total organic carbon concentration (TOC%), total nitrogen (TN%), sand
(%) and silt (%). SUM= summer, WIN= winter.
3.
Results
A summary of all Permanova results is provided in Table 1.
3.1. Environmental description
Permanova generated a significant P-value for the factor “st”, indicating that
the two sampling stations differed in terms of environmental variables. There
were no significant differences between the summer and winter sampling
periods. PCA (Fig. 2) indicated that the two stations differed mainly in
TOC% and CPE content during summer, whilst in winter there were no clear
differences.
3.2. Grain size
The The Permanova run on the silt% and sand% classes showed that
neither “st” (p = 0.0699) nor "ti” (p>0.1) were significantly different.
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Chapter IV. Temporal analysis
3.3. Sedimentary organic matter
Mean values for TOM%, TOC%, TN%, C/N and Corg/N are reported in Table
2. Only TOC% was significant at p < 0.05 (see Table 1) for the “stxti” factor.
TOM% analysis identified only a minor and non-significant influence of the
time factor “ti”, with Permanova results giving a P-value of 0.08. TN% and
C/N did not differ either between stations or seasons. TOC% varied
significantly for “stxti” (p = 0.012), with higher values at ST2 (0.69 ± 0.06 %)
compared to ST1 (0.29 ± 0.07 %) in summer (pair-wise test p = 0.0089). At
ST1 the TOC% did not vary significantly between seasons whilst it was
significantly (pair-wise test p = 0.013) higher in summer compared to winter
in ST2. TOM% showed a decrease in both stations from summer (ST1 5.22
± 0.94 %; ST2 6.09 ± 0.73 %) to winter (ST1 3.88 ± 0.38 %; ST2 3.87 ± 1.06
%).
Table 2 Sedimentary organic matter composition
TOM%
TN%
TOC%
Summer
Winter
C/N
Corg/N
0.09 ± 0.05
0.067 ± 0.01
0.29 ± 0.007
0.69 ± 0.06
10.4 ± 11.35
19.13 ± 2.71
4.42 ± 3.41
10.30 ± 0.74
3.88 ± 0.38
0.03 ± 0.01
0.35 ± 0.11
20.71 ± 5.53
11.40 ± 0.84
3.87 ± 1.06
0.03 ± 0.006
0.45 ± 0.10
15.22 ± 2.19
11.88 ± 0.91
ST 1
ST 2
5.22 ± 0.94
6.09 ± 0.73
ST 1
ST 2
Corg/N= organic carbon to nitrogen ratio; C/N is the ratio of total carbon (inorganic and organic)
nitrogen; C/N= total carbon to nitrogen ratio,Corg/N is the ratio of acidified sample’s organic
carbon content and nitrogen; TN = total nitrogen; TOC= total organic carbon; TOM% =
percentage of Total organic matter.
3.4. Pigments
Permanova identified no significant differences in CPE or phaeopigments
(Phaeo) concentrations between sampling locations or seasons.
Nevertheless, the highest average values (with the highest variances) for
both Chla and Phaeo were found at ST2 during summer (63.01 ± 25.68
Chla µg g-1 dry weight (DW) sediment and 34.43 ± 12.06 Phaeo µg g-1 DW;
see Table A7 in the Addendum). Moreover, inspection of Fig. 3 suggests
that CPE concentrations were typically much higher in ST2 than ST1 during
summer, although with large variation (97.44 ± 44.79 and 26.39 ± 4.18 µg
g-1 DW, respectively). The two sampling stations did not differ during winter
months. Permanova analysis of fucoxanthin concentrations indicated nonsignificant differences of p = 0.08 for “st” and p = 0.09 for “ti”. The highest
concentration was found at ST2 in summer (25.5 ± 13.1 µg g-1 DW).
Fibnally, when calculating the Phaeo/Chla ratio on the averaged pigment
concentration values the ratio were higher in winter than in summer, and at
ST2 compare to ST1 during the summer months (See Table A7 Addendum).
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Chapter IV. Temporal analysis
Fig. 3 Chloroplast
Pigment
Equivalents (CPE),
Fucoxanthin
concentration (µg g1
dry sediment ±
SD, left axis) and
TOC concentration
(%, right axis ± SD)
at the two sampling
stations during
summer and winter.
Values are reported
with the standard
deviation.
3.5. Meiofauna
Meiofaunal Abundance
Permanova of total meiofaunal abundances was significant for “st” and “ti”.
The two sampling stations differed from each other only during summer,
whilst ST2 showed differences between summer and winter. Higher
numbers were present in ST1 compared to ST2 during summer (12181 ±
3821 and 4681 ± 1683 ind. 10 cm-2 respectively). The total abundances at
ST2 dropped from 4681 ± 1683 ind. 10 cm-2 in summer to 1307 ± 614 ind.
10 cm-2 in winter. Nematodes were always the most abundant and
numerically important taxon, constituting 92% of the community in summer
at ST2 and 95% at ST1, while in winter their relative abundances were 98%
and 97%, respectively. Nematode abundances were about one order of
magnitude higher in ST1, with no significant differences between seasons
(Fig. 4). At ST2 there was some indication of a seasonal difference,
although the Permanova P-value was non-significant (p = 0.069).
Harpacticoid copepods (Fig. 5) showed higher abundances in summer
compared to winter, showing a p-value of 0.06. Nauplii abundance showed
a significant seasonal change (p = 0.0368), with lower numbers in winter.
Cumaceans were significantly more abundant at ST2, with no seasonal
change (Fig. 5).
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Chapter IV. Temporal analysis
Fig. 4 Nematode densities (vertical bars, numb.ind. 10 cm-2 ± SD, left y axis) at the
two sampling sites during summer and winter and nematode biomass (red rhombus,
µg C 10 cm-2 ± SD, right axis). The additional information of the mean relative genus
abundance within station was provided for each genus with no SD (names given in
legend).
Nematode genus composition
The Permanova analysis of the nematode genus composition also showed
marginally non-significant P-values for both “st” and “ti” (“st” p = 0.0621, “ti”
p = 0.0681). The nematode community genus composition is shown in Fig.
4 (as average total numbers) and Fig. 6 (as relative abundance), illustrating
differences between stations and seasons. The MDS (Fig. 7) based on
genus composition indicated that the two stations differed clearly during the
summer, whereas winter samples were less distinct (two way crossed
ANOSIM: between stations R = 0.815 p = 0.01; between times R = 0.519, p
= 0.01). The ST1 nematode community in summer was dominated by only
three genera, Aponema (38%), Daptonema (21%) and Halalaimus (15%).
ST2 showed a more even and diverse community, with the highest relative
abundance contributed by Dichromadora (18%). In winter the ST1
community was still dominated by few genera, with Halalaimus (23%)
followed by Aponema (20%) and Metalinhomoeus (12%), and ST2 was
more evenly structured, with Linhomoeus (20%) followed by Halalaimus
(15%) and Dichromadora (10%). Fig. 8 illustrates the relative abundances of
the different nematode trophic groups. ST1 in summer appeared to host a
higher relative presence of grazing genera such as the 2A feeding group,
although PERMANOVA did not identify a significant difference. Reflecting
the genus composition data, the communities at ST2 during summer and at
both stations during winter showed more even trophic composition, with
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Chapter IV. Temporal analysis
selective deposit-feeders (1A, 38%) followed by epistrate feeders (2A, 30%)
and non selective-deposit feeders (1B, 25%), and a relatively high presence
of predators (about 5%). In ST1 during summer, there was a relatively
greater abundance of epistrate-feeders (2A) (up to 60%, on average 50%)
and a very low representation of predators (2B, 0.6%).
Nematode Biomass
Nematode biomass (µg C 10 cm-2) data are presented in Fig. 4. The highest
biomass values were recorded at ST1 during summer, reaching up to 2.2
mg C 10 cm-2, although with very high variability. Biomass generally
decreased from summer to winter, more noticeably at ST1. There was a
significant difference in individual biomass between sampling stations (p =
0.0277) but not between seasons, with ST2 hosting larger nematodes than
ST1 (0.1± 0.04 µg C ind-1 in ST2; 0.04 ± 0.01 µg C ind.-1 in ST1). The
nematode “length to width” ratios (L/W) were not significantly different
between sampling stations or seasons. The average L/W values ranged
between 27 ± 11 and 33 ± 15 in ST1 and 30 ± 12 and 35 ± 19 in ST2, in
summer and winter respectively.
Fig. 5 Harpacticoid
copepod (light
brown bars), nauplii
(violet bars) and
cumacean
abundances
(numb; ind. 10 cm-2
± SD) at each
sampling site in
summer and winter.
124
Chapter IV. Temporal analysis
Fig. 6 Relative
abundance of the
most abundant
nematode genera
at the two sampling
sites in summer and
winter.
Juvenile to adult ratios
Copepods showed the highest ratio during the summer at ST2 (see Fig. 9).
No significant differences were detected between the two sampling
stations. There were significant differences (p = 0.04) in J/A ratio for
copepods between seasons, with higher values in summer (ST1 1.40 ± 0.35
in summer vs 0.30 ± 0.29 in winter; ST2 2.26 ± 0.96 in summer vs 0.01 ±
0.03 in winter). Nematode J/A ratios did not show any significant differences
between sampling stations or seasons, showing a generally constant value
of 1.13 ± 0.34.
Fig. 7 Multi
Dimensional
Scaling (MDS)
results based on
nematode genus
relative
abundances
(square root
transformed) of the
two sites (ST1 and
ST2).
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Chapter IV. Temporal analysis
Fig. 8 Trophic
composition of the
nematode
community, based
on the feeding
guilds of Wieser
(1953). The trophic
guilds codes are:
1A=selective
deposit feeders;
1B=non-selective
deposit feeders;
2A=epistrate
feeders;
2B=predators.
9 Ratios of
juvenile to adult
(J/A) for nematodes
and nauplii larvae
to copepodids (N/C
or
nauplii
to
copepodids I-V and
VI) (mean ± SD).
Fig.
4.
Discussion
4.1. Spatial differences
To clarify the possible effects of seasonality on meiobenthic community
structure at the two study sites their environmental similarities and
differences are first discussed. Granulometrically similar to one another, the
two sites differed mainly in terms of organic matter content. ST2 showed
organically richer (> TOC%, > CPE concentration, > fucoxanthin
concentration) sediments compared to ST1 during summer, whilst in winter
the concentrations were more similar, with a general decrease in TOM
content. The CPE values found in the sediments of both the sites were
comparable to those previously reported from Potter Cove (Veit-Köhler,
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Chapter IV. Temporal analysis
2005) and from the Terra Nova Bay continental shelf (Pusceddu et al.,
2000). Percentages of TOC in the current study were remarkably low (never
above 0.8%), and were lower than those found in Hornsund Fjord
(Spitsbergen, Arctic) (Grzelac & Kotwiki 2012) or in a deep sea canyon
(Ingels et al., 2011a). Despite these low TOC% values, meiofaunal
abundances were up to one order of magnitude higher than those in
Spitsbergen (Grzelac & Kotwiki 2012), and biomass showed values
comparable, if not higher, than those found in productive systems such as
an estuary (Tita et al. 2002). The higher TOC% values at ST2 were not
reflected in higher meiofauna densities or biomass.
Overall, the meiofauna showed peaks of abundance (> 10000 ind. cm -2)
comparable to others previously reported in Potter Cove (Pasotti et al., 2012
and references therein) and Signy Island (South Orkney Islands, Vanhove et
al., 2000). These values were also much higher than those reported by
Hong et al. (2011) in the adjacent Marian Cove (King George Island).
Biomass values were high (up to 2 mg C 10 cm-2), comparable to those
found in temperate estuaries (Tietjen, 1969), and up to two orders of
magnitude higher than those reported for deep-sea sites (Gambi et al.,
2010). When comparing the two study sites in terms of meiobenthic
densities and community composition, we found that they differed only in
summer, with higher values and higher number of taxa in ST1.
Differences in meiobenthos abundances have often been correlated to
sediment grain size (Skowronski & Corbisier, 2002) or organic matter
availability (Vanhove et al., 2000). However, here both stations were highly
dominated by mud (on average >80%), and no significant differences in
sediment composition were detected. When comparing the two sites during
summer, it is notable that, despite the higher food availability, the nematode
community at ST2 did not achieve higher biomass. Coull (1999), in a review
on the role of meiofauna in estuarine systems, argued that food quality
rather than quantity was a more important influence on meiofaunal standing
stocks. It is plausible that the organic matter present at ST2 was not directly
exploitable by the fauna. At ST2 during summer we had the lower
Phaeo/Chla value which indicates that Chla (fresh primary production) was
proportionally more abundant in relation to its degradation products. If we
parallel this to the higher abundance of fucoxanthin (brown/golden brown
algae presence indicator), this may explain the lack of correlation between
the higher TOC (and CPE) and the meiobenthic abundance/biomass in
these sediments. During the summer months brown seaweeds, such as
perennial Desmarestiales species, are responsible for high primary
production in Potter Cove, leading to high macroalgal biomass potentially
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Chapter IV. Temporal analysis
becoming available as detritus (Quartino and Boraso de Zaixso, 2008).
Most macroalgal primary production currently takes place on rocky
substrata along the outer part of the northern side of the cove, with some
recent evidence of colonization of newly ice-free substrata in the inner parts
of the cove (Quartino et al., 2013). While macroalgae are generally
recognized to be highly unpalatable to many organisms, they still provide a
potential carbon source through the activity of microbial decomposition
processes. Prokaryotic decomposition of available organic matter results in
lowered oxygen concentration in the sediments where these biochemical
reactions take place. Thus, the overall lower abundances of meiofauna and
the lower nematode biomass found at ST2 compared to ST1, combined with
the relatively greater presence in summer of the nematode feeding group
1A (selective deposit-feeders, 38%) at ST2 compared to ST1, could provide
further support to this hypothesis. Nematodes at both study sites showed
very high L/W values, indicating that generally slender nematodes inhabit
these sediments, which is assumed to be an adaptation to low oxygen
conditions (Jensen, 1987a).
It appears that summer macroalgal primary production in Potter Cove may
not directly stimulate the meiobenthos, and rather could negatively impact
the community by generating sub-oxic and stressful conditions within the
sediments, but further specific studies are required in order to confirm this
hypothesis. Furthermore, local differences in macrofaunal standing stocks
could play an important role in determining meiobenthos assemblage
structure (Giere, 2009).
4.2. Seasonal differences
Meiofaunal densities varied significantly between summer and winter only at
ST2. Here average winter densities decreased to half of the summer values.
A similar pattern was observed for ST1, although due to the high variances
this was not statistically significant. Biomass values for both stations
showed a significant decline from summer to winter months. Seasonal
dissimilarities were driven mainly by differences in the communities of the
two main taxa, nematodes and copepods. The reduction in total meiofaunal
densities between seasons is a pattern described by Vanhove et al. (2000)
in another Antarctic shallow water environment, and by Pawłowska et al.
(2011) in the Arctic. From our study, we can postulate that the seasonal
decrease in meiobenthos standing stocks in Potter Cove could be due (i) to
the more refractory nature of the organic matter in winter or (ii) to the likely
local decrease in oxygen concentration at the water-sediment interface due
to cessation of benthic primary production and the continuation of benthic
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Chapter IV. Temporal analysis
respiration during the winter months. Nonetheless, the relatively high
nematode densities and biomass values that were present during this
period suggest that summer primary production had been converted before
the winter months into other potential food sources (e.g. prokaryotes,
protozoan biomass or detritus). If so, the biomass reduction observed is
related to the mortality of the meiofauna itself.
The J/A ratio data obtained in this study shows that copepod larval
abundance changed with season, with significantly higher numbers present
in summer, whereas no pattern was present for the nematodes (Fig. 9). This
contrasts with the findings of a study of sub-Arctic harpacticoid species
(Steinarsdóttir et al., 2003), where the copepods brooded all year long,
again supporting a constant availability of food. This may indicate speciesspecific life strategies not investigated in the current study.
The meiofaunal seasonal abundance patterns differed among the taxa
studied. Nematodes and copepods showed lower abundance during
winter, whilst cumaceans did not show significant seasonal changes.
Nematodes are represented by various trophic guilds, some of which are
dependent on fresh material such as benthic diatoms, prokaryotes or other
metazoans (epistrate-feeders, selective deposit-feeders and predators).
Harpacticoid copepods are known to feed actively on microalgae , biofilms
or detritus, and cumaceans to feed mainly on detritus although certain
species can be predators. Pasotti et al. (2012) reported a preference for
phytoplanktonic diatom detritus compared to bacterial detritus in Potter
Cove cumaceans. The data available suggest different possible interactions
of each metazoan group with its environment, and also differences between
summer and winter seasons. Life strategies, trophic and other speciesspecific characteristics play an important role in determining meiofaunal
responses to environmental changes in Antarctic shallow water
ecosystems.
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Chapter IV. Temporal analysis
5.
Conclusions
Meiofaunal densities were generally higher in Potter Cove in summer and
lower in winter, although seasonal input of organic matter did not seem to
underlie this difference. We suggest this may be linked with the occurrence
of food-quality-related sub-oxic conditions.
Winter meiofaunal abundances were sufficiently high to infer that energy
sources are not limited during winter. This is consistent with the hypothesis
that there is no cessation in feeding, as argued by other authors for both
shallow water and shelf Antarctic ecosystems.
Recruitment in meiofaunal communities can be coupled (copepods) or
uncoupled (nematodes) to the seasonal dynamics of the cove’s sediments,
possibly linked to species-specific life history characteristics or to the
trophic flexibility of the investigated taxon.
6.
Aknowledgements
We acknowledge the ESF IMCOAST project (Impact of climate induced
glacial melting on marine coastal systems in the Western Antarctic
Peninsula region, www.imcoast.org) for financial support. FP was financed
through an IWT PhD scholarship and by Ghent University. PC is supported
by NERC core funding to the BAS ‘Ecosystems’ Programme. We thank the
Alfred Wegener Institute (Germany) and the Instituto Antartico Argentino
(Argentina) for providing logistic support at the Dallmann Laboratory in
Carlini station. Special thanks to Prof. Dr. Doris Abele and Oscar Gonzáles
for their assistance and support. We thank all the scientific and support staff
at Carlini station for their assistance in the diving and boating operations
necessary for the collection of the material described.
130
Chapter V. Tracer experiment
A resting leopard seal (Hydrurga leptonyx) and its guest (Larus
dominicanus)
“Ten percent of the big fish still remain. There are still some blue whales.
There are still some krill in Antarctica. There are a few oysters in
Chesapeake Bay. Half the coral reefs are still in pretty good shape, a
jeweled belt around the middle of the planet. There's still time, but not a lot,
to turn things around.”
Sylvia Earle
Oceanographer
(1935)
Chapter V. Tracer experiment
Adapted from:
Pasotti, F., De Troch, M., Raes, M. and Vanreusel, A.: Feeding ecology of
shallow water meiofauna: insights from a stable isotope tracer experiment in
Potter Cove, King George Island, Antarctica, Polar Biol., 35(11), 1629–1640,
2012.
Abstract
Antarctic meiofauna is still strongly understudied, and so is its trophic
position in the food web. Primary producers, such as phytoplankton, and
bacteria may represent important food sources for shallow water metazoans
and the role of meiobenthos in the benthic-pelagic coupling represents an
important brick for food web understanding. In a laboratory feeding
experiment 13C-labelled freeze-dried diatoms (Thalassiosira weissflogii) and
bacteria were added to retrieved cores from Potter Cove (15 m depth,
November 2007) in order to investigate the uptake by 3 main meiofauna
taxa: nematodes, copepods and cumaceans. In the surface sediment
layers nematodes showed no real difference in uptake of both food sources.
This outcome was supported by the natural δ13C values and the community
genus composition. In the first centimeter layer, the dominant genus was
Daptonema which is known to be opportunistic, feeding on both bacteria
and diatoms. Copepods and cumaceans on the other hand appeared to
feed more on diatoms than on bacteria. This may point at a better
adaptation to input of primary production from the water column. On the
other hand, the overall carbon uptake of the given food sources was quite
low for all taxa, indicating that likely other food sources might be of
relevance for these meiobenthic organisms. Further studies are needed in
order to better quantify the carbon requirements of these organisms.
Keywords: West Antarctic Peninsula, feeding ecology, meiobenthos, stable
isotopes
1.
Introduction
The recent global warming has increased the concern for the Southern
Ocean since Antarctic ecosystems are experiencing strong changes
(Schofield et al., 2010; Turner et al., 2005; Vaughan et al., 2003). In light of
the relatively fast rate of these changes it became of fundamental
importance to investigate and quantify the biodiversity of Antarctica whose
biota is still relatively poorly studied. Nevertheless, to understand an
ecosystem and its resilience against changes, also a more functional
approach is needed. Understanding the interactions between species and
131
Chapter V. Tracer experiment
between the different functional components of an ecosystem is therefore of
fundamental importance. In this context, tracer experiments (Maria et al.,
2011b; Middelburg et al., 2000; Moens et al., 2007) and natural stable
isotope studies (Mincks et al., 2008; Moens et al., 2007; Nomaki et al.,
2008) contribute to identify and/or to quantify the interactions between
different trophic levels. In Potter Cove, and more specifically in Antarctic
shallow waters ecosystems, this was the first time that such experimental
approach was applied.
In this study, meiofauna (or meiobenthos) refers to the group of small-sized
metazoan organisms that inhabit marine sediments and pass through a 1mm mesh size sieve and are retained on a 32-μm sieve (Heip et al., 1985;
Vincx, 1996). Meiobenthos is often numerous and diverse. Past studies
suggested that these metazoans are involved in the sediment organic
matter remineralization (Coull, 1999) and contribute to the overall benthic
carbon flux (Szymelfenig et al. 1995), and they have been considered as an
important link in marine food webs. More recent tracer experiments indicate
microalgae and bacteria as possible meiofauna food sources (Evrard et al.,
2010; Ingels et al., 2010b; Urban-Malinga and Moens, 2006). Nevertheless
the measured 13C uptakes often showed not to be enough to cover the
expected carbon requirements of certain meiofauna taxa (e.g. for
nematodes in Urban-Malinga and Moens, 2006; Franco et al., 2008; Guilini
et al., 2010; Ingels et al., 2010 and for copepods in De Troch et al., 2005),
suggesting the importance of preference for food sources other than those
provided in the experiments. On the other hand, other authors (Coull, 1999;
Nyssen et al., 2002) have stated that meiofauna may play an important role
in transferring carbon to the higher trophic levels being prey for many other
organisms, mainly juvenile fishes. These conflicting results underline the
numerous uncertainties in meiofauna feeding habits and their role in trophic
webs. Moreover in extreme environments, such as Antarctica, there is an
even bigger lack of relevant information to unravel the trophic position of
meiofauna, which is one of the reasons this study was undertaken.
In the present study we focus on the feeding ecology of Potter Cove
meiofauna. Potter Cove (62°14'S, 58°40'W, King George Island, West
Antarctic Peninsula) is an Antarctic fjord-like small embayment (~3 km2)
with a max. depth of 50 m and influenced by the Fourcade Glacier (Fig. 1).
Since the 50’s the glacier has been actively retreating (Rückamp et al.,
2011) in response to the air warming trends of the West Antarctic region
(Schofield et al., 2010; Vaughan et al., 2003). So far, the meiobenthic
community of this cove has been studied mainly in terms of densities, major
taxonomic composition (Mayer, 2000; Veit-Köhler et al., 2008), and
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Chapter V. Tracer experiment
abundances of copepods and their biovolumes in relation to environmental
conditions (Veit-Köhler, 2005). However, despite its high abundance, a
more functional approach to unravel the trophic position and its possible
contribution to the benthic food web is lacking so far. The present work
would be the first such investigation in this remote environment.
Fig.1 Maps showing the location of the study site: a) the map shows the area of the
tip South America and the Antarctic Peninsula indicating in the circle King George
Island as part of the South Shetland Islands, Northern tip of the West Antarctic
Peninsula; b) the map shows King George Island (62° 14’ S, 58° 40’ W) indicating
with the arrow the location of Potter Cove; c) the map shows Potter Cove and the
black dot represents the study site.
With the present study we wanted to investigate the uptake by 3 chosen
meiofauna taxa when provided with phytoplanktonic algae or benthic
bacteria as potential food sources. Phytoplankton has been highly studied
in Potter Cove. In fact, the cove is characterized by frequent high
turbulence and high water column turbidity which lead to relatively low
primary production (PP) in the water column (Schloss and Ferreyra, 2002;
Schloss et al., 2002). Anyhow, in light of the strong warming of the average
air temperatures occurring in Potter Cove during the last 50 years, the cove
ecosystem is facing visible changes. Melt water flow is a constant
phenomenon during summer months (Eraso and Dominguez, 2007), and
the Fourcade glacier is actively retreating (Dominguez and Eraso, 2007).
On the local scale, water column stabilization and more intense
phytoplankton blooms are expected to represent part of the effects that are
likely to occur because of these climate-related changes (Dierssen et al.,
133
Chapter V. Tracer experiment
2002; Schloss et al., 2002; Smith and Nelson, 1985; Turner et al., 2005),
leading to an increasing importance of the phytoplankton contribution to
these sediments’ food input.
In addition to sinking phytoplankton cells, also microphytobenthic diatoms,
sea-ice algae and macroalgal fragments are potential constituents of the
sediment’s organic matter pool on which the detritus pathway is based.
Bacteria can play an important role in the detritus pathway especially in the
winter months when the summer production is accumulated in the
sediments and is likely to be transferred to higher trophic levels (e.g.
meiofauna organisms and other detritivores) via microbial reworking
(Nedwell et al., 1993). In this work we therefore focused on both
phytoplanktonic diatoms and benthic bacteria as possible food sources for
the meiobenthos.
The main questions of this tracer study can be resumed as follows: 1) is
there a different uptake of bacteria and phytoplanktonic diatoms by
meiofauna over time? and 2) do the main taxa differ in terms of uptake of
the given food sources?
2.
Materials and Methods
2.1. Sampling site and experimental design
The sampling site was located in Potter Cove in front of the Fourcade
Glacier (see black dot in Fig. 1), at a depth of about 15 m, where fine sand
soft bottoms were suitable for scuba diving sampling. A total of 18 sediment
push cores (5.6 cm inner diameter, 24.62 cm2 surface) were retrieved at the
beginning of the austral summer (November 2007) in the same day over an
area of about 5 m2. As control (natural carbon isotopic signature of
metazoans) 3 replicate cores were sliced (0 - 1, 1 - 2 cm) and stored frozen
(- 80°C); 3 extra replicates were sliced (0 - 1, 1 - 2, 2 - 3, 3 - 4, 4 - 5 cm)
and stored in 4% formaldehyde for meiofauna community analysis. In
addition, 12 cores were collected to serve as experimental units in the
laboratory experiment.
Prior to the sampling campaign, diatoms and bacteria were grown and 13C
pre-labelled to be used as food sources in a tracer experiment. The
planktonic diatom species Thalassiosira weissflogii (strain CCMP1587, 1418 µm length, 8-10 µm width) was selected for this experiment. The diatoms
were reared in 2L erlenmeyers with f/2 culture medium (Guillard, 1975, 30
psu) where 5 ml of a NaH13CO3 solution (336 mg in 100 ml milliQ H2O) was
added per 100 ml of the culture medium. After 3 weeks of growing at 20 °C
and on a 12-h: 12-h light/dark light regime, the algae passed from an initial
δ13C signature of -15.9‰ (Atm% 1.1) to an enriched value of 47491.9‰
134
Chapter V. Tracer experiment
(average Atm% 35.3) for untreated and enriched cultures, respectively.
Bacteria from Schelde estuary’s sediments (at Belgium-The Netherlands
border) were initially grown on marine agar for 4 days at 15-16°C. In order
to maximize the bacterial diversity in the inoculum, a dilution series was
setup (protocol by Moens Tom, Ghent University). The liquid growth
medium consisted of autoclaved artificial seawater (24.5 PSU, Instant
Ocean synthetic salt), Beef extract (DIFCO, 3 g L -1) and Bactopeptone
(DIFCO, 5 g L-1). Two erlenmeyers were inoculated with the bacterial mix
scraped from the agar plates and placed on a shaking table at room
temperature. After 3 days of growth, new growth medium was prepared as
stated above but diluted by a factor 20 and 0.5 g L -1 13C glucose (Dglucose, U-13C6, 99%, Cambridge Isotope Laboratories, Inc.) was added to
label the bacteria. After 24-h of growth this labeling technique yielded an
increase in δ13C from -15.2‰ (Atm% 1.1) to 70268.9‰ (average Atm%
44.5), for untreated and 13C enriched cultures, respectively. After sufficient
growth, both cultures were washed with autoclaved filtered natural seawater
and freeze dried.
A total of 12 single-food source experimental units were incubated in a
controlled water bath at +1°C constant temperature, including triplicates of
two treatments (food source) for two time intervals: Diatoms 5 days, Diatoms
10 days, Bacteria 5 days and Bacteria 10 days. The rather limited
experimental time was constrained by the mission limits in terms of
permanence time frame (three weeks) at the base (taking into account as
well of the weather conditions) during the austral summer 2009/2010.One
aliquot of freeze-dried food source (diatoms or bacteria) was added to each
core and the water surface was gently stirred until all food settled on the
sediment surface. Each core was provided with 30 mg of freeze-dried
material which corresponded to about 8-9 mg C per core. All cores were left
open at the top and were oxygenated with an air pump. This experiment
was carried out in the dark to avoid primary production. After the incubation
period the first two centimeters (0 - 1, 1 - 2 cm) of the sediment were sliced,
collected into Petri dishes and stored frozen (- 80°C) pending further
analysis. Here we report only the uptake results for the first two centimeters
for the nematodes since they contain the majority (> 50 %) of the total
meiofauna community and because in absence of sediment stirring the
label may not have penetrated deeper than that. Moreover harpacticoid
copepods and cumaceans were only found in the upper layer in sufficient
biomass to conduct reliable stable isotope analyses.
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Chapter V. Tracer experiment
2.2. Meiofauna processing and statistical analysis
Extraction of meiofauna from the 4% formaldehyde preserved samples
followed standard procedures of centrifugation-flotation with LUDOX HS40,
and sieving over 1000 and 32 µm sieves (Heip et al., 1985; Vincx, 1996).
Meiofauna taxa identification was based on (Higgins and Thiel (1988). We
identified the nematodes at the genus level. The identification was carried
out by collecting 100 individuals randomly from each replicate of each layer
of sediment and then mounting them on glass slides. The online
identification key for free-living marine nematodes (NeMysKey©) developed
within Nemys (http://nemys.ugent.be/), and the identification key by
Warwick et al. (1998) were used. For the nematode biomass determination,
standard methods were used by the estimation of body volume using
Andrássy’s formula (Andrássy, 1956): V = L x W2/16x · 105, where V is the
volume in nanoliters, L is the length in µm (excluding filiform tails, if present)
and W is maximal width in µm. Body volume was converted to biomass (μg
wet weight 10 cm-2) assuming a specific gravity of 1.13 (Wieser, 1960) and
a dry/wet weight (DW/WW) ratio of 0.25. Biomass was then converted to
carbon assuming a dry weight/µg C ratio of 0.124 (Jensen, 1984). In this
way nematode biomass could be measured for all depth layers. Biomass
(μg C 10 cm-2) of copepods and cumaceans was estimated based on the
stable isotope μg C values (see further) by multiplying the individual
average biomass with the total number of individuals per 10 cm 2 of the 0 - 1
cm layer of natural community samples.
Possible dissimilarities in terms of meiofauna densities and nematode
biomasses between sediment depth layers were investigated through
ANalysis Of SIMilarities and the ANalysis of SIMilarities PERcentages
(ANOSIM and SIMPER, Primer-E, ltd, version 6.1.6).
2.3. Stable isotope analysis
The frozen sediment of both control and experimental cores was thawed
and meiofauna was elutriated via Ludox HS40 and sieved as for the
community analysis (Heip et al., 1985; Vincx, 1996). The use of ludox was
not expected to have any effects on the stable isotopic signatures of the
organisms as demonstrated in previous studies (Moens et al., 2002).The
extracted meiofauna was transferred into milliQ (MQ) water in sterile Petri
dishes and directly processed in order to avoid potential leakage of label
(see Moens et al., 1999; Mourelatos et al., 1992). About 150 nematodes, 15
cumaceans and 30 harpacticoid copepods have been separately
handpicked with a fine sterile needle, rinsed twice in MQ water to remove
adhering particles, and finally transferred to a drop of MQ water in 2.5 x 6
136
Chapter V. Tracer experiment
mm Al cups. The cups had been preheated at 550 °C to remove any
contaminating organic carbon. The Al cups with the animals were then
oven-dried overnight at 60 °C, pinched closed, and stored in air-tight multiwell microtiter plates. The carbon isotopic composition of the samples was
determined with a PDZ Europa ANCA-GSL elemental analyser 230
interfaced to a PDZ Europa 20-20 isotope ratio mass spectrometer (Sercon
Ltd.,
Cheshire,
UK;
UC
Davis
Stable
Isotope
Facility,
http://stableisotopefacility.ucdavis.edu/).
Uptake of 13C is reflected as excess (above natural abundance) 13C and is
expressed as total uptake in the sample (I) in µg C (quantitative) and as
specific uptake Δδ13C (Δδ13C = δ13Csample - δ13Ccontrol) in parts per thousands
(‰) (qualitative), according to (Middelburg et al., 2000). δ13Csample is
calculated as [(Rsample - RVPDB) / RVPDB] x 103 with RVPDB = 0.0112372 = the
carbon isotope ratio of the Vienna Pee Dee Belemnite standard, and Rsample
= [(δ13Csample / 1000) + 1] x RVPDB (Craig, 1957; Middelburg et al., 2000).
Fractional abundance of 13C (F) equals R/(R + 1) and is used to calculate
the excess 13C (E) in the samples, which is the difference between the 13C
fraction of the sample (Fsample) and the 13C fraction of the control (Fcontrol): E
= Fsample - Fcontrol.. I is here calculated as the product of E and C weight (μg)
of each sample (as measured in the isotope analysis results). Since we
added 2 different food sources, uptake values (I) have been corrected
according to their initial level of label incorporation. The uptake has been
reported as 1) individual uptake (I per ind., µg 13C ind-1), which can show
differences between the taxa due to their individual biomass, 2) a
standardized uptake expressed per unit of biomass ( I per unit C, µg 13C C-1)
and the 3) I per total number of ind. core-1 which was calculated by
multiplying I per ind. values with the average total abundances in the
corresponding first cm depth layer (Fig. 5).
Significant differences in Δδ13C, and the biomass specific uptake (I per unit
C) were investigated by means of a three-way analysis of variance (3-way
ANOVA) on the rank values with the Statistica [version 7.0] software
(StatSoft. Inc., 2001). Results are reported indicating p values and F values.
The values for each factor’s degrees of freedom are 1 for food, 2 for taxa
and 1 for time. N depends on the combination of factors. In case of the 3way ANOVA N = (3 replicates x 3 taxa x 2 food sources x 2 incubation
periods) = 36. A posteriori comparisons were carried out with the Tukey’s
HSD test using 95% of confidence limits. Prior to the ANOVA, the Levene’s
test was used to check the assumption of homogeneity of variances only in
case raw data were used.
137
Chapter V. Tracer experiment
3.
Results
3.1. Meiobenthic community
The meiobenthic community was characterized by total abundances
ranging from 3671 to 10873 ind. 10 cm-2 (Fig.1). The dominant taxon was
nematodes (91%), followed by nauplii (and copepodites) (5.4%) and
harpacticoid copepods (2.1%). Nematode abundances (0-5 cm) showed a
high variability between the three replicates ranging from 3339 to 10409
ind. 10 cm-2, with an average value of 6010 ind. 10 cm-2. In the upper
layers, nematodes were found in average densities of 2643 and 5186 ind.
10 cm-2, in the 0-1 and 1-2 cm layer, respectively.
The average abundance of copepods was 115 ± 16 ind. 10 cm-2 (mean ±
SD). Among the other metazoans, cumaceans were the most important
(0.6% of total abundance), showing relatively high abundances with an
average value of 29 ± 11 ind. 10 cm-2 (mean ± SD). Up to 41 specimens per
replica have been counted, and 90% of them were confined in the upper
centimeter. Polychaetes (0.3% of total abundance) were important too and
were present in almost all sediment layers analyzed. Other meiofauna
groups present were Hydrozoa, Amphipoda, Isopoda, Ostracoda and
Bivalvia, representing together on average 0.23% of the total meiobenthic
abundance over the 5-cm depths analyzed (but the taxa were present only
in the 0-2 cm layer).
In general, the total nematodes’ biomass in the top layers (0 - 5 cm) (Fig. 3)
showed an average value of 482.98 ± 350.84 µg C 10 cm -2 (mean ± SD). In
the 0-1 and 1-2 cm sediment layer, nematodes showed average biomass
values of 74.45 ± 34.63 and 158.91 ± 102.79 µg C 10 cm-2 (mean ± SD),
respectively. Increasing mean individual body sizes towards the deeper
layers indicated the presence of higher relative abundances of large
nematodes (i.e. Metasphaerolaimus, Sabatieria, Metalinhomoeus).
Copepods’ biomass in the first layer of the sediment was 93.37 ± 117.55 μg
C 10 cm-2 (mean ± SD), and cumaceans accounted for 127.07 ± 50.50 μg
C 10 cm-2 (mean ± SD).
The nematode assemblage conisted of 44 genera in total. Table 1 shows
the most abundant genera and their corresponding trophic guilds. The
genera Daptonema, Aponema, Amphymonhystrella and Halalaimus were
the most abundant accounting together for > 60% of the total nematode
community. Vertical distribution of the various nematode genera illustrated a
gradual depth gradient in terms of genus presence/absence and relative
abundances, with the intermediate layers forming a transition zone in terms
of community structure between the surface (0 - 2 cm) and the deeper
138
Chapter V. Tracer experiment
layers (3 - 5 cm) (table 2). The ANOSIM results confirm these findings
(factor = cm depth; R = 1) with a significance level of p < 0.002. The
nematode genera Daptonema, Dichromadora and Anticoma were abundant
in the upper layer (0 - 1 cm) and showed a clear drop in densities toward
the deeper sediment layers. Amphimonhystrella, Retrotheristus and
Aponema increased in importance in the intermediate sediment layers
which coincides with peaks in total nematode abundances. Sabatieria and
Metalinhomoeus were characteristic for the deeper layers (3 - 5 cm).
Fig.2 Vertical
density profiles of
meiofauna taxa
(mean ± standard
error).
Fig. 3 Vertical
distribution of
average nematode
biomasses in _g C
10 cm-2 (mean ±
standard deviation)
139
Chapter V. Tracer experiment
Table 1 Relative abundances (%) of nematode genera in the first two centimeters
layer (left part of the table) and in the total community (0–5 cm). TG= trophic group
Genus
0-1
cm
Genus
1-2
cm
Genus
0-5
cm
TG
Daptonema
45.09
Aponema
31.55
Aponema
31.1
2A
Halalaimus
13.03
Halalaimus
17.12
Daptonema
13.8
1B
Dichromadora
6.91
Daptonema
9.16
Amphimonhystrella
12.7
1B
Aponema
5.4
Desmolaimus
8.97
Halalaimus
12
1A
Anticoma
4.58
Amphimonhystrella
7.12
Desmolaimus
4.37
1B
Prochromadorella
3.56
Trichotheristus
4.53
Dichromadora
3.31
2A
Acantholaimus
2.66
Chromadorita
3.86
Metasphaerolaimus
2.68
2B
Metasphaerolaimus
2.66
Retrotheristus
3.32
Trichotheristus
2.66
1B
Desmolaimus
1.88
Dichromadora
3.15
Metalinhomoeus
2.66
1B
Paramonhystera
1.68
Acantholaimus
2.1
Chromadorita
1.79
2A
Amphimonhystrella
1.19
Metasphaerolaimus
1.37
Retrotheristus
1.76
1B
Trichotheristus
1.19
Aegialoalaimus
0.89
Acantholaimus
1.43
2A
Chromadorina
1.13
Wieseria
0.74
Anticoma
1.33
1B
Metalinhomoeus
1.04
Leptolaimus
0.71
Prochromadorella
1.01
2A
Chromadorita
0.97
Anticoma
0.56
Sabatieria
0.87
1B
Neochromadora
0.97
Linhomoeus
0.56
Linhomoeus
0.7
1B
Mesacanthion
0.85
Oxystomina
0.52
Oxystomina
0.65
1A
Microlaimus
0.69
Gnomoxyala
0.4
Paramonhystera
0.59
1B
Retrotheristus
0.69
Prochromadorella
0.4
Aegialoalaimus
0.54
1A
Halomonhystera
0.63
Chromadorina
0.37
Neochromadora
0.51
2A
Trophic groups (Wieser 1953) legend: 1A = selective deposit feeders, 1B = nonselective deposit feeders, 2A = epistratum feeders,2B = predators/omnivores
140
Chapter V. Tracer experiment
Table 2 Relative abundances (%) of the most important genera showing the vertical
zonation of these genera.
Genus
0-1 cm
1-2 cm
2-3 cm
3-4 cm
4-5 cm
Trophic guild
Daptonema
45.09
9.16
3.02
1.76
1.76
1B
Dichromadora
6.91
3.15
1.9
0.37
0.4
2A
Anticoma
4.57
0.55
0.31
0
0
1B
Halalaimus
13.03
17.12
8.4
3.25
8.71
1A
Aponema
5.4
31.55
41.62
56.5
17.28
2A
Retrotheristus
0.69
3.31
1.35
0
0
1B
Amphimonhystrella
1.19
7.12
26.34
13.51
4.08
1B
Metalinhomoeus
1.03
0
4.27
9.82
15.79
1B
Sabatieria
0
0.18
1.08
2.42
24.81
1B
Desmolaimus
1.88
8.97
1.8
2.42
1.66
1B
Metasphaerolaimus
2.66
1.37
3.9
2.5
8.46
2B
Acantholaimus
2.66
2.1
0.31
0
0
2B
ANOSIM showed the following groups: upper layer zone (0-2 cm, light grey), an intermediate
zone (1-4 cm, darker grey) and a deep zone (3-5 cm, very dark grey). The genera contributing
most to this dissimilarity and to the similarity within each group, as indicated by SIMPER, are
highlighted.
Table 3 Results of a 3-way ANOVA analysis performed on the ranked values of
the Δδ13C, I per individual and I per unit carbon.
Factors
Δδ13C
In per ind.
F
p
F
food
41.6395
0.000001
147.51
taxon
10.5764
0.000509
226.51
time
12.8517
0.001493
food*taxon
0.8487
food*time
taxon*time
food*taxon*time
I per unit C
p
F
p
0
20.377
0.000143
0
24.657
0.000045
17.143
0.000369
7.5792
0.002809
0.44043
9.505
0.000912
0.2057
0.815529
1.3627
0.275061
0.171
0.682522
0.0906
0.766051
0.3681
0.54976
2.057
0.149765
0.2057
0.815529
0.9612
0.396667
0.514
0.604369
1.4283
0.259371
F values and p values are reported for food (bacteria and diatoms), taxon (nematodes,
copepods and cumaceans) and time (5 and 10 days) and for all the combinations of these
three factors. Significant p values (p < 0.05) are highlighted in bold font.
141
Chapter V. Tracer experiment
a
b
c
Fig.4 (a) Δδ13C (in, ‰), (b) I per ind. (μg 13C ind-1) and (c) I per unit carbon (μg 13C μg
C-1) for 3 meiofauna taxa (see legend) in the 0-1 cm depth (mean ± standard error).
142
Chapter V. Tracer experiment
Fig.5 Total uptake I
(μg 13C) of bacteria
and diatoms by
nematodes,
copepods and
cumaceans (total
number of individuals
per core) in the 0-1
cm layer (mean
values).
Fig.6 I per unit carbon
(μg 13C μg C-1) of the
nematode community
in two different layers
(0-1 cm and 1-2 cm
depth) (mean ±
standard error).
3.2. Stable isotope signatures
Background δ13C average values (natural stable 13C ratios) for the studied
meiobenthic taxa were as follows: nematodes -19.35 ± 1.37‰, copepods 17.89 ± 0.53‰, and cumaceans -14.57 ± 0.32‰. The natural stable
isotopic signatures point at some trophic differentiation between the 3
chosen taxa (1-way ANOVA p < 0.05).
The results of a 3-way ANOVA analysis based on the Δδ13C ranked values
for the experimental results are summarized in table 3. All factors of interest
(time, taxon and food) had a significant effect on the specific uptake values.
Based on the Δδ13C values (Fig. 4 a), copepods and cumaceans showed at
each time interval a higher uptake of diatoms in comparison with bacteria
(Fig. 4 a, Tukey’s HSD test: p < 0.01). Nematodes, however, did not show
any significant difference in Δδ13C values for both food sources (Tukey’s
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Chapter V. Tracer experiment
HSD test: p > 0.05). Nematodes also showed a slower response to the
enrichment with both food sources since only after 10 days of incubation
their uptake was appreciable.
Standardization towards individual uptake values ( I per ind.) yielded a
statistically significant difference between both food sources with a higher
consumption of the diatom Thalassiosira weissflogii by all tested taxa (Fig. 4
b). Uptake of bacteria has been recorded as well for all groups but was
lower than that of the phytoplankton food source for each taxon. In the first
sediment layer (0-1 cm), there was a clear difference in terms of individual
uptake between the different taxa, with Cumacea showing higher values for
both food sources when compared to nematodes at each time interval
(Tukey’s HSD: p < 0.01). In comparison to copepods, cumaceans showed a
higher individual uptake just after 5 days and only when feeding on bacteria
(Tukey’s HSD: p < 0.01). Further standardization towards I per unit C (Fig. 4
c) aimed at illustrating possible differences in the C assimilation from the
13
C-labelled sources by the different taxa. However, despite the significant
level of variance of the 3-way ANOVA for the I per unit C (Fig. 4c), the Post
Hoc analysis did not show any significant difference in the assimilation of
the two different food sources or in the assimilation between the different
groups (Tukey’s HSD p > 0.05).
Based on the contribution of each taxon to the uptake of the food sources
(see Fig. 5), it was observed that after 10 days the three dominant taxa
together consumed a total of ~4.2 μg C from 13C-labelled source per 10 cm2
or 9.3 μg C from 13C-labelled diatoms core-1; and a total of 0.72 μg C from
13
C-labelled source per 10 cm-2 or 1.68 μg C from 13C-labelled bacteria
core-1. These values mean that after 10 days the nematodes, copepods and
cumaceans together took up 0.39% and 0.04% of the total 13C carbon from
diatoms and bacteria, respectively. After 5 days, nematodes alone took up
0.01% and 0.002% of diatoms and bacteria respectively, while at the end of
the experiment they showed a total uptake of about 0.09% and 0.01% of the
C present in the 13C-labelled diatoms and bacteria standing stock.
Comparing nematodes of both sediment layers (0-1 cm versus 1-2 cm) (see
Fig.6) it was clear that the labelled food sources were not very accessible in
the subsurface layer since a delayed response can be noticed and higher
overall uptakes were shown in the upper centimeter layer community.
Again, the nematodes did not show a significant (1 way ANOVA p > 0.05)
preference for any of the two given food sources.
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Chapter V. Tracer experiment
4.
Discussion
4.1. Meiofauna community standing stocks
The total meiofauna abundances of this site were high compared to
temperate shallow water ecosystems (Vanhove et al., 1998 and
comparisons therein; Leduc and Probert, 2010). (Veit-Köhler et al. (2008)
found similarly high densities between 10 and 20 m water depth (up to
16835 ind. 10 cm-2) in Potter Cove. In agreement with our results,
nematodes were the most abundant taxon followed by copepods (including
nauplii), cumaceans and annelids. The first meiofauna study in Potter Cove
by Mayer (2000), however, showed much lower meiobenthos densities
(maximum densities of 485.5 ind. 10 cm-2 at a depth of 10 m) in comparison
with Veit-Köhler et al. (2008) and the present study. However, similar high
abundances (and high between replicate variances) have been recorded in
other Antarctic areas by Vanhove et al. (1998, 2000) (Factory Cove South
Orkney Islands, Antarctica, average 6200 ind. per 10 cm -2) and in Martel
Inlet (Admirality bay, KGI, by de Skowronski et al., 1998, densities between
3523 and 8216 ind. 10 cm-2, and by de Skowronski and Corbisier, 2002,
densities between 1953 and 6310 ind. 10 cm-2). It is important to state that
abundance data are also dependent on the mesh size range used during
the investigation, and unfortunately not always the same mesh size sieve
are widely used (e.g. Skowronski et al., 1998, used 500- and 68-µm sieve).
This can make comparisons more difficult. Anyhow, the high abundances
suggest that food is not limiting in shallow water Antarctic bottoms, and
micro-scale differences in the sediment characteristics, such as primary
production (microphytobenthos and macroalgae), secondary (bacteria and
protozoans) production processes and sediment granulometry (de
Skowronski and Corbisier, 2002; de Skowronski et al., 2009; Vanhove et al.,
2000; Veit-Köhler et al., 2008a) may lead to high spatial heterogeneity.
4.2. Nematode community, diversity and structure
The dominant nematode genera in the investigated Potter Cove station were
Daptonema and Aponema. Both genera were also reported by Vanhove et
al. (1998, 2000) representing more than 60% of the nematodes assemblage
at Factory Cove. In general, the assemblage found in the present study
appears to be similar, at family level, to those found in other shallow
meiobenthic communities in subtidal fine sands worldwide (Heip et al.,
1985; Juario, 1975; Vanreusel, 1990), with a dominance of genera
belonging to the families Xyalidae (Daptonema), Monhysteridae (e.g.
Amphimonhystrella) and Microlaimidae (e.g. Aponema) and a community
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Chapter V. Tracer experiment
trophically represented by the dominance of non-selective deposit feeders
and epistratum feeders (Wieser, 1953).
In the surface layer Daptonema, which is classified as a non- selective
deposit feeder (group 1B), dominates the community representing almost
half of it in terms of abundances. It is well known as an “opportunistic
genus” (Vanhove et al., 2000) because it shows a particular preference for
diatoms as food source but can easily switch to bacteria. Daptonema can
be stated to be a very flexible genus having been positively correlated with
the pico- and nano-fraction of water pigments (so to say
phytoplankton,Vanhove et al. 2000), and with microphytobenthos (Moens et
al., 2005) and moreover it has been observed to feed on small ciliates
(Moens and Vincx, 1997). As a result, an opportunistic genus that is
capable to feed on different food sources seems to be successful, also in
Antarctic shallow waters. Moreover, Schratzberger et al. (2000) reported for
two North Sea species of Daptonema a high resistance to the temporal
absence of food, which may indicate that beside the feeding plasticity this
genus may have evolved the capacity to survive in conditions of starvation.
Aponema (an epistrate feeder) became more dominant in the 1-4 cm layer.
It is possible that being capable of fast vertical migrations (Schratzberger et
al., 2000) this genus could still benefit in the subsurface layer of the
presence of food on top of the sediment, and at the same time avoid
surface predation.
4.3. Trophic ecology
The natural carbon signatures of the three meiofauna taxa analyzed in the
present study were compared with data on the food sources taken from
(Corbisier et al., 2004), Kaehler et al. (2000) in view of the similarities in
terms of biota and environmental characteristics of these Antarctic sites.
The natural carbon signatures of the possible food sources (from the works
by Corbisier et al., 2004 and Kaehler et al., 2000) ranged from the more
depleted values of phytoplankton (around -25‰) to those of
microphytobenthos and macroalgae (from around -16‰ to around -23‰).
Cumaceans during our study showed the highest δ13C values, with an
average value of -14.57‰. There is still not much known about the feeding
ecology of cumaceans. This taxonomic group includes families with large
differences in morphological characteristics which in turn create a wide
range of feeding strategies within the order. Cumaceans of shallow water
environments in the Antarctic are primarily known as deposit feeders
(feeding for instance on organic matter and microorganisms) but able to
graze on epipelic algae growing on sand grains (Blazewicz-Paszkowyczi
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Chapter V. Tracer experiment
and Ligowski, 2002). However, there are also examples of predatory
behavior among members of few families (e.g. Nannastacidae and
Gynodiastylidae), which have piercing mandibles and may prey on
polychaetes and foraminiferans (Blazewicz-Paszkowyczi and Ligowski,
2002; Brusca and Brusca, 2003; Kozloff, 1990). Comparing these values
with the results of our feeding experiment (where cumaceans showed they
feed more on diatoms than bacteria), we could support the idea that this
taxon feeds on detritus (e.g. algal material with associated diatoms) both in
a direct (selectively) and in an indirect (e.g. feeding on bacteria that
degrade detritus) way, although additional food sources may play a role
too.
Copepods showed an average δ13C value of -17.89‰. Copepods are
known to feed on both microalgae (benthic and planktonic) and bacteria
(directly or from a biofilm), which can lead to different species-specific
isotopic signatures (Nascimento et al., 2008; De Troch et al., 2005; UrbanMalinga and Moens, 2006). On the other hand, the tracer experiment
showed a higher uptake of planktonic diatoms with values (both I per ind.
and I per unit C) laying within the range of those measured during various
experiments performed on different temperate copepods’ species under
laboratory conditions (De Troch et al., 2005, 2006; Wyckmans et al., 2007).
Anyhow, copepods from our study showed a much lower I per unit C
compared to their temperate counterparts, as reported by Maria et al.
(2011b). In this study, the authors found uptake as high as 0.7 µg c µg C -1
when the small crustaceans were given benthic-labelled diatoms. The use
of benthic diatoms was not planned in our experiment, but future studies in
Potter Cove should focus also on this component of the benthic primary
producer biota. In terms of food quality, diatoms are known to synthesize
polyunsaturated fatty acids (PUFA) that are important metabolic
compounds that animals cannot synthesize de novo (Tocher, 2003).
Bacteria can contain a large variety of fatty acids but normally produce very
small amounts of ω-3 and ω-6 PUFA (Brett et al., 2009 and references
therein). So far, it remains unclear whether grazers’ selectivity is based on
food quality or on other factors as e.g. particle size (De Troch et al., 2006)
and food concentration (De Troch et al., 2007). The fact that labelled
diatoms uptake remained anyhow low can be possibly explained by the fact
that 1) other non-labelled diatoms were also present in the experimental
cores and 2) the studied taxa feed more specifically on benthic diatoms
than on phytoplanktonic species.
Nematodes showed an average stable δ13C signal of -19.35‰, which
appears to be more depleted than the δ13C values reported for the
nematode community in Martel Inlet (δ13C = -15.6 ± 0.7‰) by (Corbisier et
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Chapter V. Tracer experiment
al., 2004) but heavier than the values (δ13C = -24.8 ± 1.3‰) found for
Bransfield Strait shelf (230 m depth) communities (Moens et al., 2007).
These natural stable isotope values seem to point to a predominance of
pelagic carbon sources in the nematodes diet in Potter Cove. These may be
related to a delayed response of nematodes (uptake of already reworked
labelled food sources) or to the use of other food sources. From literature
nematodes are known to potentially feed on bacteria that may degrade
sedimentary detritus (e.g. macroalage) and also on microphytobenthos.
Accordingly, nematodes’ responses to our feeding experiment confirm
these previous findings: they feed similarly on both given food sources,
bacteria and microalgae. The nematode community in our study was
dominated by Daptonema in the first cm layer, which can exploit the diverse
available food sources (bacteria and/or benthic/phytoplanktonic diatoms
and/or ciliates) present in the cove sediments, supporting all year round
relatively high nematodes’ densities as observed in a temporal study on
Signy Island in similar conditions (Vanhove et al., 2000). In Corbisier et al.
(2004b) nematodes were significantly linked to microphytobenthos as a
food source. Microphytobenthos may be an important food source also in
Potter Cove, but up to now a lack of information about its abundance and
biomass within the cove is hampering possible inferences on its role as
food for benthic organisms analysed in the present study.
The delayed response of nematodes observed in the experiment has also
been reported before for deep-sea (Ingels et al., 2010b; Witte et al., 2003)
and the Antarctic shelf (Moens et al., 2007) communities. However this
result is in contrast with what Moens et al. (2002) found in a temperate
estuarine tidal flat, where nematodes have been reported to
consumelabelled microalgae already in the first 3 h of the experiment. Our
result may indicate that, as mentioned before, (1) the labelled carbon
entered the animals indirectly (e.g. feeding on bacteria that already had
grown on the labelled diatoms or on protozoans that fed on them), or that
(2) the nematodes of these Antarctic shallow water sediments have a slower
response to the input of new carbon, and 3) organisms were not hungry
because of high background organic carbon (Braeckman et al., 2011b)
present (about 4.7% of sediment dry weight in summer months, Pasotti data
not published). If we compare our surface nematode community with that of
a temperate sandy beach (Maria et al. 2011b), it was noticed that
interestingly the I per unit C values from our experiment are in the same
order of magnitude of those that Maria et al. (2011b) found for the 1B
community group, in this case feeding on labelled benthic diatoms. In
contrast our community total uptake per unit of organism is much lower than
reported by Maria et al. (2011b) reported for the 2A feeding group
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Chapter V. Tracer experiment
(epistratum feeders) community. In fact our community in the first cm layer
was dominated for 45% by Daptonema, a genus belonging to the 1B group.
The dominance of a detritus feeder community may lead to lower direct
uptake of microalgae which may on the other hand be taken up via detritus
after reworking by other organisms (see also Moens et al., 2002). In general
after 10 days, the nematode community still did only incorporate about
0.09% of the 13C label in the diatom food source. This is a relatively small
amount (2 orders smaller) in comparison to a shallow water North Sea
nematode community where after 2 weeks 1.29% of the given labelled
Skeletonema costatum inoculum was taken up (as recalculated from Franco
et al., 2008). Antarctic shelf nematodes collected at 230 m water depth and
fed with cyanobacteria, only took up ~ 0.03 % of 13C in the bacterial food
after 10 days (Moens et al., 2007). This illustrates that the nematodes from
Potter Cove respond similarly as the Antarctic shelf community, at least in
terms of uptake, responding in the same order of magnitude (i.e. < 0.1%) to
the given food sources (bacteria in Moens et al., 2007 or diatoms in this
study). Up to now most of the experiments aimed at tracing the uptake of
labelled food sources in meiofaunal taxa have found that these animals do
not seem to fulfill the expectations on carbon cycling and benthic
mineralization despite the fact that they are given the food sources they
supposedly consume. These findings may point at different plausible
reasons: 1) the food sources given in the experiments are not in a state that
is appetible for the animals (fresh cells vs freeze-dried ones, see Cnudde et
al., 2011); 2) the competition for food with other organisms, not taken into
account during the analyses (e.g. macrofauna), may be underestimated.
The lower nematodes’ uptake in the deeper sediment layer may indicate
that the food needed more time to reach these strata, however, due to the
high variances between replicates no statistically significant difference was
found. The scarce penetration of added labelled food to deeper layers in
laboratory sediment cores has been reported already by other authors
(Ingels et al., 2010; Middelburg et al., 2000; Moens et al., 2007). Additional
factors in the experimental setup that may interact with the food uptake that
was actually measured, include the background presence of organic matter
in the test sediment, the presence of other organisms and the use of freezedried food sources.
5.
Conclusions
Despite the fact that the natural stable isotopic signatures pointed at some
trophic differentiation between the 3 dominant taxa of the Potter cove
meiofauna, no striking differences in assimilation were shown between
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Chapter V. Tracer experiment
these taxa by means of lab enrichment experiments in which selected prelabelled bacteria and pelagic diatoms were used. However copepods and
cumaceans showed at each time interval a higher uptake of diatoms in
comparison to bacteria, whereas nematodes did not show any significant
difference in uptake for both food sources.
The relatively high dominance of an opportunistic genus such as
Daptonema (which can feed on many different food sources) supports this
less selective feeding behaviour of the nematode community.
Nematodes also showed a slower response to the enrichment with both
food sources since only after 10 days of incubation their uptake was
appreciable. Possibly there is a lower direct uptake of microalgae which
may on the other hand be taken up via detritus after reworking by other
organisms.
However, overall our experiments showed that after 10 days the nematodes,
copepods and cumaceans together took up only 0.4 % and 0.04% of the
total 13C carbon from diatoms and bacteria, respectively. This observation
can have different causes but may point to the fact that other food sources
play a significant role.
The overall contribution of nematodes to the remineralisation of
phytoplanktonic carbon in Potter Cove appears to be limited compared to
other temperate regions, but it is higher than shown for Antarctic deep-sea
environments. On the contrary, the uptake of bacteria is similar to that of
deep-sea communities, and again it shows how nematodes feed on this
food source to a very limited extent.
In conclusion we can state these three shallow water Sub-Antarctic
meiofauna taxa may depend on the overlying water column, but still their
low uptake does not seem to mirror their putative carbon requirements.
Their contribution to the reworking of the given food sources appeared too
low to be considered essential to the potential overall sediment carbon flux.
Whether other food sources are more important for their diet or the given
food sources were not in a state that was appetizing for the animals, or
whether the presence of other organisms (e.g. macrofauna organisms) in
the experimental unit did have an influence on the selected meiobenthic
taxa uptake needs further investigations.
6.
Aknowledgements
We acknowledge the ESF IMCOAST project (Impact of climate induced
glacial melting on marine coastal systems in the Western Antarctic
Peninsula region, www.imcoast.org) and the SDD-BIANZO (Biodiversity of
three representative groups of the Antarctic Zoobenthos: coping with
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Chapter V. Tracer experiment
change) project (Belgian science policy) for financial support. The first
author financed through an IWT PhD scholarship. The second author was a
postdoctoral fellow of the FWO-Flanders Research Foundation (Belgium) at
the time of the experiment and is now financed by the Ghent University
(BOF-GOA 01GA1911W). We also thank the Alfred Wegener Institute
(Germany) and the Instituto Antartico Argentino for providing the logistics at
Dallmann laboratory in Jubany station. A special thank goes to Prof. Doris
Abele for her precious assistance during the set-up of the experiment. Last,
but not least, we would like to thank Dr. Nicole Aberle-Malzahn and Dr.
Evangelia Gontikaki for their valuable help given in revising the present
work.
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Chapter VI. Sedimentation and selectivity
experiments
Elephant seals in harem - Mirounga leonina
“A place where it's possible to see the splendours and immensities of the
natural world at its most dramatic and, what's more, witness them almost
exactly as they were, long, long before human beings ever arrived on the
surface of this planet. Long may it remain so.”
David Attenborough
Naturalist
(1926)
Chapter VI. Sedimentation and selectivity experiments
Pasotti F., De Troch, M. and Vanreusel, A.: “To cope or not to cope?” Can
Antarctic meiofauna cope with impacts from glacier-retreat? Insights from
two laboratory experiments.
Abstract
The West Antarctic Peninsula is experiencing severe changes in regional
climatic conditions. Locally, glacier retreat leads to changes in marine
coastal environments due to higher incidence of ice-growlers scouring,
enhanced inorganic sedimentation, the appearance of newly ice-free
substrates and alterations in primary producers’ equilibria. The effects of
these changes on the Antarctic organisms have been object of several field
studies. In this study we investigated two aspects of climate change by
means of laboratory experiments: i) the effect of inorganic sedimentation
(SED) on the vertical distribution of the meiofauna and ii) the effects of
sediment displacement and different types of food (SEL) on the composition
of meiobenthic and nematode assemblages in surface sediments. In the
SED experiment the experimental setup (the use of closed plexiglass cores)
resulted in an upward movement of the nematodes, while no other effects of
the sediment load were detected. In the SEL experiment the mechanical
disturbance mimicked during the collection of the natural sediment caused
significant losses in the densities of nauplii and copepods, which may have
escaped or showed to be sensitive to this type of disturbance. Among the
nematode assemblage, Aponema had an overall increase in relative
abundance in the experimental units, benefiting of the sediment mechanical
re-working during sampling. The different kinds of detritus given in the
microcosm (shredded macroalgae, the benthic diatom Seminavis robusta
and the haptophyte Isochrysis galbana) did not result in significant
differences among treatments in terms of meiofauna composition at higher
taxon level. The nematode assemblage however, was dominated by
epistrate feeders (2A) in the control and the Seminavis robusta treatments
resembling the natural background nematode assemblage. The
macroalgae and the haptophyte detritus seemed to stimulate the presence
of non-selective deposit feeders (1B). The genus Sabatieria reached the
highest relative abundance in these samples compared to both the other
treatment and the background sediments, possibly because of increased
hypoxic conditions in the presence of this type of detritus. Unfortunately, the
high variances found in the experimental units hindered the finding of
unequivocal effects on the nematode assemblages in both experiments.
Keywords: meiofauna, nematodes, glacier retreat, experiment, West
Antarctic Peninsula
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Chapter VI. Sedimentation and selectivity experiments
1.
Introduction
The Antarctic, and especially the West Antarctic Peninsula, is undergoing
strong environmental shifts in relation to recent climate change (Clarke et
al., 2007; Convey et al., 2009b; Thomas et al., 2013; Turner et al., 2013a).
Locally warmer summer air temperatures have led to conspicuous glacier
retreat (Cook et al., 2005) and related glacial meltwater runoff, which in turn
can release big amounts of inorganic and organic particles coupled to fresh
water inputs. This affects water column properties such as turbidity and
salinity (Dierssen et al., 2002), and can have a cascading effect on both the
water column and benthic organisms. Freshening conditions have been
reported to cause shifts in the Antarctic phytoplankton community from an
assemblage dominated by large diatoms to one where smaller
phytoplanktonic components are more abundant (Moline et al., 2004). The
size range composition of the phytoplankton assemblage is very important
because it largely determines which part of the freshly produced biomass
can be passed on to the local higher trophic levels given the consumers
community composition. Moreover, the collapse of parts of a tidewater
glacier tongue can uncover and make available new substrata for
colonisation of macroalgae and related fauna (Quartino et al., 2013), having
a potentially local positive effect on the overall production of seaweed
biomass.
Meiofauna organisms (32-1000 µm size range) are a very diverse metazoan
group, which plays a pivotal role in the benthic compartment enhancing
remineralisation (Bonaglia et al., 2014) and serving as food for higher
trophic levels (Coull 1999 and references therein; Giere, 2009). In the site
under study, Potter Cove (PC, King George Island, West Antarctic
Peninsula), shallow water meiofauna was highly abundant (Pasotti et al.,
2012, 2014b; Veit-Köhler et al., 2008a) and influenced by the local
conditions in relation to the glacier front (Pasotti et al., 2014b; Veit-Köhler et
al., 2008a). Here a tidewater glacier has been retreating since the 1950’s
and several parts of the northern coast, including a small island, became
ice-free and are undergoing macroalgal colonisation (Quartino et al., 2013).
During the summer months the meltwater streams of the glacial rivers
generate low salinity/high turbidity waters in the inner part of the cove. The
innermost river can discharge in the cove up to 30 g m -2 d-1 of inorganic
particles (Ferreyra et al., 2003), and this ongoing high sedimentation has
caused shifts in the distribution of differently adapted ascidian species in
the past decades (Sahade et al., 1998; Torre et al. 2014). The majority of
meiobenthic organisms lack a larval stage and hence they are tightly linked
to the sediments in which they are living (Giere, 2009) while they are also
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Chapter VI. Sedimentation and selectivity experiments
Fig. 1.Overall
map of the
Antarctic
Peninsula
with the
location of
King George
Island (a),
Potter Cove
(b) and the
investigated
site (c) within
Potter Cove
directly affected by water column processes. Enhanced inorganic
sedimentation has been reported to influence the distribution of
meiobenthos in an Arctic fjord (Grzelak and Kotwicki, 2012), whereas in PC
the meiofauna seemed relatively well adapted to this type of events, while
temporarily suffering from disturbances from growler scouring or from
oxygen stress in relation to local organic load (Pasotti et al., 2014b). In this
study the responses of the meiobenthos to three main events were
investigated by means of two experiments: i) a sedimentation experiment
(SED) to study the possible effects of inorganic sedimentation on the
distribution (e.g. vertical density profiles) and composition of the meiofauna
and ii) a combined food selectivity - disturbance experiment (SEL) to study
the possible effect of mechanical disturbance (e.g. growler scouring
sediment reworking), coupled to the presence of different types of detritus
(macroalgae, benthic diatoms and small haptophytes) on the structure of
the surface sediment meiofauna and nematode assemblages. Our
questions are: 1) does inorganic sedimentation affect the distribution and
survival of meiofauna taxa? and 2) do mechanical disturbance and/or food
quality influence the composition of meiobenthic and nematode
assemblages?
2.
Material and Methods
2.1. Sampling site and experimental design
The two experiments were set up in the Dallmann laboratory of the
Argentinian/German land research base “Carlini” (former Jubany) situated
in Potter Cove (see map in Fig.1, King George Island, West Antarctic
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Chapter VI. Sedimentation and selectivity experiments
Peninsula). Samples for the experiments were collected by divers in
February 2010 at 15 m depth at station7 (also called Faro site, 62° 22' 57.2"
S, 58° 66' 76.9"W). For the analysis of the natural meiobenthic assemblage
structure, three perspex push cores (5.4 cm inner diameter, 22.89 cm2
surface area) were collected at the site and sliced in 0-1, 1-2, 2-3, 3-4 and
4-5 cm layers right after being brought to the laboratory. These background
samples were fixed and stored in formaldehyde 4% (buffered with prefiltered seawater) until processing.
Sedimentation experiment (SED): this experiment aimed at investigating the
possible effects of inorganic sedimentation on structural and functional
aspects of meiobenthic communities. A total of eighteen cores were taken
during the same dive as the background samples were collected. These
cores were transported immediately to the laboratory where they were
immersed into two buckets (9 cores each) filled with ambient seawater kept
at in situ temperature conditions (0° ± 2° C SD). Cores were closed on top
to prevent evaporation, while air was gently bubbled with aeration tubes in
the overlying water to avoid oxygen depletion but without causing sediment
re-suspension. The cores were incubated in the lab at the natural
photoperiod regime for one to two weeks. The experiment consisted of
three treatments: i) control (Ctrl, no treatment), ii) inorganic sediment added
on top (S), and iii) inorganic sediment with a fresh food source added (one
local phytoplankton species, SP). Each treatment was randomly triplicated
within the buckets. The treatments were sampled after one week and two
weeks collecting independent cores. The inorganic sediment added on top
of the sediment cores was obtained by muffling (500 °C for 6 hours) in situ
sediment and grinding it to a finer matrix. We added a total of 7 grams per
core (22.89 cm2 surface area) which equals to 116 days of the maximum
sedimentation rate (30 g m-2 d-1) measured at the mouth of melt water river
formed during the summer in the inner part of Potter Cove (Ferreyra et al.,
2003). The pre-muffled sediment was evenly distributed on top of the
sediment of both S and SP treatments in a layer of about 2 mm. To the SP
treatments we also added aliquots (5 ml of a culture with a concentration of
1 µg Chla L-1) of fresh detritus of Porosiras glacialis, a phytoplanktonic
diatom species common in Potter Cove, isolated from water samples and
cultured in the weeks prior to the experiment. At the end of the incubation,
the cores were sliced in 0-1, 1-2, 2-3, 3-4 and 4-5 cm layers and the
sediment fixed in 4% formaldehyde (buffered with pre-filtered seawater)
until processing.
Mechanical disturbance and selectivity experiment (SEL): the aim of the
experiment was to understand the impact of mechanical disturbance (such
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Chapter VI. Sedimentation and selectivity experiments
as that from growlers scour) coupled to presence of different food quality
(type of detritus) on the structure of meiofauna and nematode assemblages.
The experiment was run in a microcosm set up: a container (75 cm lenght *
50 cm width * 50 cm height) was filled with in situ collected (by dragging a
bucket by divers) sediment covered with ambient seawater. The bucket was
immersed in a water bath to keep temperature as constant as possible and
close to in situ conditions (0°C ± 2°C). The sediment was left to settle for 48
hours and the visible epibenthic macrofauna (e.g. scale worms) was
removed by hand. The overlying water was aerated with means of air
pumps and air diffusers. Syringes of 3.5 cm inner diameter were put in the
sediment with their tip cut-off. They had two opposite lateral holes (8 cm
height * 2.5 cm width) which were also immersed into the sediment till the
top level of the hole reached the water-sediment interface. Both holes were
covered with a net of 300 µm mesh size in order to allow horizontal
migration of the meiofauna and maintain lateral interstitial flow. Each syringe
aliquot was enriched with one of three different types of detritus: i) freezedried Seminavis robusta (~50 µm cell length, benthic pennate
Bacyllariophyceae), ii) frozen Isochrisys galbana (4-8 µm cell diameter,
phytoplanktonic Haptophyceae) and iii) shredded stranded intertidal
macroalgae detritus (Palmaria decipiens). Control units were also present
and had no detritus added. The microalgae were cultured in the laboratory
prior to the campaign, whereas the macroalgae were collected along Potter
Cove shores. The strain S. robusta was provided by the Phycology and
Aquatic Ecology Laboratory (PAE, Ghent University), whereas I. galbana
was a purchased axenic strain (CCMP1323). The experiment was run for
one week and two weeks starting at the time of the addition of the detritus.
The experiment was terminated by taking out the syringes with the sediment
and replacing them by small plastic beakers of equal diameter as the
syringes to prevent the sediment from collapsing. The first 0-2 cm of the
sediment inside the syringe were used for the analysis of meiofauna
densities and nematode trophic guilds. Samples were stored in
formaldehyde 4% (buffered with pre-filtered seawater) until further
processing.
For all samples, meiofauna was extracted from the sediment matrix
following the standard procedure of centrifugation-flotation with LUDOX
HS40, and sieving over 1000- and 32-µm sieves (Heip et al., 1985; Vincx,
1996). For all the sediment samples (background, SED and SEL) meiofauna
taxa were identified (on three replicates except for the Seminavis robusta
samples where one replicate was lost) based on (Higgins and Thiel, 1988).
For the SEL experiment two replicates of the first time period of each
treatment were used for nematode genera identification. Randomly, 100
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Chapter VI. Sedimentation and selectivity experiments
individuals per replicate were picked and mounted on glass slides. The
identification key by (Warwick et al., 1998) and the online identification key
for free-living marine nematodes (NeMysKey©) developed within Nemys
(http://nemys.ugent.be/) were used for the identification of nematode
genera, whereas Wieser (1953) was used for the trophic guild identification.
3.
Statistical analysis
Meiofauna densities were square root transformed prior to the statistical
analysis. Nematode genera and trophic guilds (Wieser, 1953) were
analysed as relative abundances without further transformation.
In the sedimentation experiment (SED) we wanted to test for differences in
the meiobenthic community structure (vertical distribution, taxon richness
“S” and evenness “J”) i) between the experimental units (as a whole, no
specification of detritus added or not) and the background samples
(experiment effect, EE) and ii) within the different experimental units
(treatment effect, TE). We used non-parametric permutational ANOVAs
(Permanova). To test for the experimental conditions effect (EE) we used a
fully crossed three-factor design with random factor replicate “re” nested in
the fixed factor time “ti” (background vs experimental units), next to the
fixed factor layer “la”. The interaction terms “ti x la” informs on the possible
effects that the experimental conditions had on the vertical distribution of
meiofauna. To test for effects of the experimental treatments (TE) we used a
fully crossed four-factor design with random factor replicate “re” nested in
the fixed factor treatment “tr” (the two treatments S and SP and the control
C), next to the fixed factor layer “la” next to the fixed factor time “ti” (time 1
week and time 2 weeks). The interaction term “tr x la” informs about the
possible specific effects of the treatments on the vertical distribution of the
organisms. The interaction “tr x ti” highlights possible effects of time on the
specific effects of a treatment. We used a nested design since data from
different depth layers from a single replicate core are not fully independent.
W ran these nested designs in a PERMANOVA which is equivalent to a
univariate ANOVAs with p-values obtained by permutation (Anderson and
Millar, 2004). When only a restricted number of permutations was possible
in the pairwise tests, p-values were obtained from Monte Carlo samplings
(Anderson and Robinson, 2003). Bonferroni’s correction was applied before
interpreting the multiple pairwise results correcting the p-value based on
the number of pair-wise tests (n) carried out (Bonferronip = 0.05/ n). The
PERMDISP routine was performed to test for the homogeneity of dispersions
(Anderson, 2006).
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Chapter VI. Sedimentation and selectivity experiments
In the mechanical disturbance and selectivity experiment (SEL) we tested
for i) the possible effect of mechanical disturbance on the composition of
meiofauna (composition, taxa richness “S” and evenness “J”) and
nematode assemblage, and ii) the effect of different detrital food sources
on both the meiobenthic higher taxa and nematode genera (composition
and richness “S”). For this purpose we used again non-parametric
permutational ANOVA (Permanova). A fully crossed two-factors design was
used to test the mechanical effect with fixed factor time “ti” and the random
factor replicate “re” nested in treatment. The experimental units were
considered as a whole, with “Time 0” corresponding to the background
conditions and “Time 1” and “Time 2” representing the controls and
experimental units together at each corresponding time period. When
testing the possible effects of the specific detritus treatments on the
assemblage structure, we used a fully crossed three factors design, with
the random factor replicate “re” nested in the fixed factor treatment “tr”
together with the fixed factor “time”. The p-values for the pair wise tests
were obtained from Monte Carlo samplings (Anderson and Robinson 2003)
in case of insufficient number of possible unique permutations. As
previously mentioned, Bonferroni’s correction was applied before
interpreting the multiple pairwise results correcting the p-value based on
the number of pair-wise tests (n) performed (Bonferronip = 0.05/ n). The
Permdisp routine was avoided due to small (n < 5) sample size (Anderson
et al., 2008), therefore a multi-dimensional scaling (MDS) was performed in
order to visually examine the position of the samples in an ordination plot
and infer about the nature of the possible differences detected by the
Permanovas. Moreover, the non–parametric method of the analysis of
similarities (ANOSIM) was coupled to the Permanova in order to confirm
statistically significant differences highlighted by the permutational Anova.
4.
Results
Permutational Anova results and pair-wise comparison tests results are
reported in Table 1.
4.1. Background meiofauna assemblage
Meiofauna at the study site (Fig. 2) was represented by a total of 18 taxa
and showed an average total density on the 0-5 cm depth profile of 1288 ±
297 ind. 10 cm-2 (variance of 23%). The highest values (avg. 511 ± 65 ind.
10 cm-2) were reported for the subsurface (1- 2 cm) layer, and the 0-2 cm
layer comprised always more than 65% of the total 0-5 cm layer
assemblage densities. Nematodes dominated the assemblage with an
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Chapter VI. Sedimentation and selectivity experiments
average relative abundance of 87%, followed by nauplii and harpacticoid
copepods, both taxa showing an average relative abundance of about 4%.
Fig. 2 Natural (Station 7, or Faro site) meiobenthos densities (number of individuals
10 cm-2 ± SD) along a vertical profile (0-5 cm depth) for nematodes (above) and
other important taxa (below).
The nematode assemblage of the 0-2 cm layer consisted of 52% epistrate
feeders (2A), followed by non-selective deposit feeders (37%) (see Fig. 3).
Dichromadora was the most abundant genus (avg. 22.83%) followed by
Daptonema (17.57%) and Chromadorina (13.22%) (see Table 2). The
meiofauna taxa richness (S) in the cores at the two time intervals (Time 1
and Time 2) differed significantly from that of the background samples
(Time 0) but only for the deeper layer 2-3 cm (see Table 1). Nematodes
dominated the 0-5 cm depth profile (> 75%) community in all the
experimental units, followed by nauplii and harpacticoid copepods, with no
significant differences in terms of evenness J’ neither between background
conditions and treatments nor between the three different treatments
(controls “C”, only sediment “S” and sediment and Porosiras glacialis “SP”)
and no time effect was detected. Variances (var) in the meiofauna 0-5 cm
depth profile densities were relatively high within the experimental cores
(C1var = 32% and C2 var = 29%; S1 var = 34% and S2 var = 30%; SP1 var
= 56% and SP2 var = 40%).
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Chapter VI. Sedimentation and selectivity experiments
Fig. 3 Nematodes trophic guilds (Wieser, 1953) for the natural conditions (station 7)
and the selectivity experiment SEL treatments after one week incubation. The trophic
guilds are: 1A= selective deposit feeders; 1B = non selective deposit feeders; 2A =
epistrate feeders; 2B = predators/omnivors.
4.2. Sedimentation experiment (SED)
The meiofauna taxa richness (S) in the cores at the two time intervals (Time
1 and Time 2) differed significantly from that of the background samples
(Time 0) but only for the deeper layer 2-3 cm (see Table 1). Nematodes
dominated the 0-5 cm depth profile (> 75%) community in all the
experimental units, followed by nauplii and harpacticoid copepods, with no
significant differences in terms of evenness J’ neither between background
conditions and treatments nor between the three different treatments
(controls “C”, only sediment “S” and sediment and Porosiras glacialis “SP”)
and no time effect was detected. Variances (var) in the meiofauna 0-5 cm
depth profile densities were relatively higher within the experimental cores
(C1var = 32% and C2 var = 29%; S1 var = 34% and S2 var = 30%; SP1 var
= 56% and SP2 var = 40%) than those found in natural background
conditions. The highest densities for nematodes, nauplii and copepods
were recorded in replicates from the SP1 treatment where the maximum
value of 4288 ind. 10 cm-2 in the 0-5 cm depth profile was counted together
with the highest above mentioned variances.
The vertical profiles of the meiofauna showed the highest densities in the 01 cm layer with a steep decline towards the deeper layers in all treatments
(see Fig. 4 a and b for the most abundant taxa nematodes, harpacticoid
copepods and nauplii). This pattern differs from that found in the natural
conditions since no subsurface (1-2 cm) density peak was present, as
confirmed by a significant permutational Anova and related pairwise tests
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Chapter VI. Sedimentation and selectivity experiments
p-values (see Table 1). Permdisp analysis confirmed (p = 0.934) that the
differences observed with the Permanova analysis were not due to the
dispersion of variances but because of real differences between groups. No
significant differences in the meiobenthos vertical profiles were found
between the S and SP treatments and the controls at both times.
4.3. Mechanical disturbance and selectivity experiment
(SEL)
The higher taxa composition of the 0-2 cm layer meiofauna community of
both the background and the experimental unit samples are represented in
Fig. 5. The Permanova analysis on the richness “S” that tested for the
experimental setup effect (the mechanical disturbance) showed significant
differences between the background conditions and the microcosm
conditions (see Table 1). On the other hand, the pair-wise comparisons
showed differences between Time 0 (background or natural values) and
both the experimental treatments (Time 1 and Time 2) with p<0.05, but not
to a p-value level small enough for the Bonferroni correction applied (for
comparisons n=3, Bonferroni corrected p ≤ 0.016). To better interpret this
result we performed an MDS on a Euclidean distance-based matrix built on
the “S” values (Addendum, Fig. A5). In the MDS it is possible to appreciate
two distinct groups based on the factor “ti”, but no real possible distinction
can be made based on the factor “tr” (among the experimental units). The
permutational Anova of the meiobenthos community “S” between the
different detritus treatments and the control at each time did not yield any
significant result. The same pattern was shown by the Permanova carried
out for the evenness index ‘J’ of the meiofauna, with the sole difference
where the pair-wise comparisons gave p-values closer to or lower than
(hence significant) the Bonferroni corrected p-value 0.016 (see Table 1).
Harpacticoid copepods and their nauplii larvae showed significant effects
(pair-wise also significant for Time 0 compared to both Time 1 and Time 2)
from the mechanical disturbance but no effect of the different food detritus
treatments. The nematode assemblage after one week incubation was
trophically dominated by epistrate feeders (2A) in the Control (56.65%) and
Seminavis robusta (58%) treatments, whereas non-selective deposit feeders
were dominant in the Macroalgae (47.23%) and Isochrysis galbana
(45.39%) experimental units (see Fig. 3).
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Chapter VI. Sedimentation and selectivity experiments
Fig. 4 Sedimentation experiment (SED) densities (n° individuals 10 cm -2 ± SD) vertical
profiles of nematodes, nauplii and copepods after 1 week incubation (left) and two
weeks incubation (right) with three treatments: i) control (dark grey bars), ii) only
inorganic sediment (black bars), iii) inorganic sediment with added aliquots of live
Porosiras glacialis (light grey bars). In the nauplii graph on the right the standard
deviation (SD) bar for the light grey bars only shows the negative value of the SD.
This was done in order to hold the same axis values in between the one week and the
two weeks treatments for all the taxa.
Dichromadora was the dominant nematode genus in the Control (29.88%),
I. galbana (16.80%) and S. robusta (24.75%) samples, whereas in the
Macroalgae treatments Sabatieria (22.30%) appeared to be the most
abundant genus (see Table 2 for more details). Aponema increased in
importance in all the experimental units compared to the background
samples, with a relative abundance ranging from 14.36% ( I. galbana) to
17.82% (S. robusta), compared to 4.03% in the background sediments.
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Chapter VI. Sedimentation and selectivity experiments
Fig. 5. Selectivity experiment (SEL) meiofauna higher composition taxa (n° individuals
10 cm-2 ± SD) in the surface layer (0-2 cm) of the natural condition (station 7) and
experimental treatments (control, macroalgae, Isochrisys galbana and Seminavis
robusta). The experiment was run for one week and two weeks.
5.
Discussion
5.1. Sedimentation experiment SED
A change in the vertical profile of the meiobenthic community, mainly
dominated by nematodes, was observed between the in situ natural
background conditions and the experimental conditions samples, but not
between the different treatments. The main difference consisted in the
disappearance of the subsurface nematode density peak at the 1-2 cm
layer, and the establishment in the experimental setup of a steep vertical
density profile with the highest nematode abundances in the first
centimetre, the layer where the inorganic sediment was added. It appears
that the nematodes moved from the subsurface 1-2 cm layer to the surface
layer, whereas no clear differences were highlighted for the deeper layers.
The possible explanation for such an upward movement could be the lack
of surface predation which in natural conditions would generate an
avoidance reaction (Giere 2009) and push the assemblage to move in
deeper layers. The use of closed isolated cores for the experiment
eliminated the effect of the vagile megafauna normally present in situ which
may be exploiting the nematofauna by selective or non-selective epistratum
feeding. What we observed in the experimental units was somehow
unexpected: despite the non-statistically significant differences compared
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Chapter VI. Sedimentation and selectivity experiments
to the controls, the sediment “S” and “SP” treatments presented the highest
densities of nematodes, copepods and nauplii after one week. Seen the
potential negative effects of fine inorganic sediment on the filtering activities
of copepods and the dilution factor on the available food sources (see
further), these results contradict the expectations. After two weeks the
densities of copepods and nauplii in the treatments levelled off with those of
the control treatments. Nevertheless, the high small-scale patchiness of the
in situ community and the resulting high variances found in the experiment
may shade possible patterns in the meiobenthic responses. Interestingly
the addition of food in the sedimentation treatment “SP” presented the
highest number of individuals to be counted and also the highest variances
to be recorded, increasing the uncertainty in the interpretations, but
pointing at a possible positive effect of the fresh phytoplanktonic detritus for
nematodes, copepods and their larvae.
Vertical distribution patterns of meiobenthos depend on a variety of biotic
(e.g. predation, food availability etc., Giere, 2009) and abiotic (oxygen
availability, sediment instability, ice scour etc. Giere, 2009; Moodley et al.
2000, Urban-Malinga et al. 2005) factors. The dependence on certain
environmental conditions, such as food or oxygen availability, is however
taxon-specific. Copepods are normally limited to the top layer in sediments
as they are highly sensitive to oxygen depletion (Coull 1970; Moodley et al.,
2000; Giere 2009). Nematodes, on the other hand, seem to be less sensitive
to oxygen profiles but vertically migrate in relation to organic matter content
and mixing activity by macrofauna (Braeckman et al., 2011a, 2011b;
Moodley et al., 2000; Vanreusel et al., 1995). Further, high inorganic
sedimentation rates such as those resulting from intense glacial discharges
can have deleterious effects on the filtration performances of
macroepibenthic filter-feeders (Torre et al., 2012). Fine sediment particles
can be responsible for the clogging of the filtering apparatus of
harpacticoid copepods (De Troch et al., 2005) and when falling in high
amounts on the sediment surface, they may have a dilution effect on the
overall food available in the first centimetre. In Potter Cove, summer
meltwater streams can turn into rivers that discharge in the cove up to 18-30
g m-2 day-1. Sediment load can be locally enhanced by the frequent
turbulent mixing re-suspension of fine material during storms (up to 30 m
depth (Schloss et al., 1999). During our experiment we added about 116
days (7 g on 22.89 cm2) of inorganic load for the sediment treatments as
one single extreme event. We realise this is rather a non-natural extreme
condition, and we therefore expected to see dramatic changes in the
composition, densities and vertical profiles of the meiobenthic organisms
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Chapter VI. Sedimentation and selectivity experiments
between our controls (no sediment addition) and the sediment treatments.
But this was not the case in this investigation.
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Chapter VI. Sedimentation and selectivity experiments
Table 1 Permanova results of the two experiments: a) sedimentation b) mechanical stress and selectivity experiment. Treat= treatment; Ti = time; La
=layer.; NA = not applicable; ns = not significant; R(nest) =replicate nested in a specific factor (see Material and methods for details).
PERMANOVA p < 0.05
PAIR WISE comparison-Bonferroni corr. p = 0.05/n
A) Sedimentation experiment
Meiofauna densities
square root transformed
Bray Curtis
Treat
Time
Layer
R(nest)
Ti x la
Treat
x la
NA
0.032
0.0001
ns
0.0006
NA
Significant pairwise
(factor "ti" n= 3) Time 0 vs Time 1 p= 0.0005 ; Time 0 vs Time 2
p= 0.003
Experiment effect
(factor "la", n = 3) layer 1-2 cm Time 0 vs Time 1 p= 0.0078 And
Time 0 vs Time 2 p=0.0002
Treatment effect
ns
ns
No
test
Species richness "S"
ns
ns
ns
NA
Euclidean distance
No transformation
Treat
Time
Layer
R(nest)
Ti x la
Treat
x la
NA
0.0392
0.0001
0.002
ns
NA
Significant pairwise
factor "ti" has no significant pair-wise
Experiment effect
factor "la" : Time 0 vs Time 1 AND Time 2 layer 2-3 cm p<0.006
Treatment effect
ns
ns
ns
ns
Treat
Time
Layer
R(nest)
Ti x
la
Treat x la
Significant pairwise
Experiment effect
ns
ns
ns
ns
ns
NA
NA
Treatment effect
ns
ns
ns
ns
NA
ns
NA
Evenness "J"
NA
ns
NA
Euclidean distance
No transformation
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Chapter VI. Sedimentation and selectivity experiments
Table 1 Continued
B) Mechanical disturbance and Selectivity experiment
Meiofauna densities
square root transformed
Treat
Time
Layer
R(nest)
Mechanical effect
NA
0.046
ns
NA
Detritus effect
ns
ns
ns
ns
Treat
Time
Layer
R(nest)
NA
0.0124
ns
NA
Meiofauna taxon Richness "S"
Mechanical effect
Bray Curtis
Tix la
Treat x la
Significant pairwise
Time 0 vs Time 1 p= 0.003
not transformed
Euclidean distance
Ti x la
Treat x la
Significant pairwise
Time 0 vs Time 1 p=0.0416 * cfr MDS
Time 0 vs Time 2 p=0.024 * cfr MDS
Detritus effect
ns
-
ns
Meiofauna Evenness "J"
ns
not transformed
Treat
Time
Layer
R(nest)
Mechanical effect
NA
0.018
ns
NA
Detritus effect
ns
-
ns
ns
Euclidean distance
Ti x la
Treat x la
Significant pairwise
Time 0 vs Time 1 p=0.0168
Time 0 vs Time 2 p=0.002
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Chapter VI. Sedimentation and selectivity experiments
Table 1 Continued
Nauplii
not transformed
Treat
Time
Layer
R(nest)
Mechanical effect
NA
0.03
0.03
NA
Detritus effect
ns
ns
ns
NA
Treat
Time
Layer
Copepods
Bray-curtis similarity
Ti x la
Treat x la
Time 0 vs Time 2 p=0.0055
not transformed
R(nest)
Significant pairwise
Time 0 vs Time 1 p=0.0002
Bray-curtis similarity
Ti x la
Treat x la
Significant pairwise
Time 0 vs Time 1 p=0.0047
Mechanical effect
NA
0.02
ns
NA
Detritus effect
ns
ns
ns
NA
Treat
Time
Layer
R(nest)
Mechanical effect
ns
0.034
NA
NA
NA
Detritus effect
0.02
ns
ns
ns
ns (dispersion of variances) - (ANOSIM R=0.71 )
Treat
Time
Layer
R(nest)
Mechanical effect
NA
ns
ns
NA
Detritus effect
0.02
ns
ns
ns
Nematode genera
Time 0 vs Time 2 p=0.0014
relative abundances
Nematode Trophic Guilds
Bray-curtis similarity
Ti x la
Treat x la
relative abundances
Significant pairwise
Euclidean distance
Ti x la
Treat x la
Significant pairwise
ns (dispersion of variances)
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Chapter VI. Sedimentation and selectivity experiments
In general from this experiment it seems that inorganic sedimentation as
such has no effect on the vertical distribution of the most abundant taxa of
this shallow water Antarctic meiofauna, suggesting that other more
important biotic (e.g. predation) or abiotic (e.g. ice-scour) factors may be
involved.
5.1. Mechanical disturbance and selectivity experiment
(SEL)
The Antarctic environment is strongly governed by seasonality in climatic
conditions. Each austral summer icebergs can break off from the
glaciers/ice shelves and strong inputs of fresh primary production replenish
the marine environment. Ice disturbance (e.g. ice scouring and anchor ice)
in Antarctic shallow waters represents the major structuring force for the
benthos (Brown et al., 2004; Convey et al., 2012; Gutt, 2001) and its action
has been described as more destructive to benthic communities than
temperate region’s fishing activities (Brown et al., 2004). Food availability
and inter-annual variability have been ascribed as responsible for the
feeding plasticity of certain macrobenthic groups (Peck et al., 2005; Tatián
et al., 2008) and the fluctuations in standing stocks of Antarctic meiofauna
(Pasotti et al., 2014a; Vanhove et al., 2000). The mechanical disturbance
exerted during the retrieval of the in situ sediment affected the surface (0-2
cm layer) meiobenthic assemblage in terms of diversity (reduced diversity
in the experimental units, nematodes dominant taxon by > 90%) but not for
total meiofauna densities. This result differs from the observations of Lee et
al. (2001a) where a shallow water (8-9 m depth) ice scour reduced the local
meiofauna densities by 95%. This would point to the fact that the
experimental retrieval of the sediment did not mimic realistically an ice
scour. In fact, the action of the sediment retrieval would more likely have
resulted in a surface community displacement together with the sediment.
In the microcosm right after retrieval, microphytobenthos was highly
abundant on the sediment surface. The almost absence of the harpacticoid
copepod group and the nauplii larvae in the microscosm could have two
possible explanations: i) the copepods, being very vagile organisms,
avoided to be caught or ii) these taxa are sensitive to this type of sediment
displacement and their mortality was significantly high. Sreedevi (2008)
observed enhanced abundances of both nematodes and copepods in a
tropical shallow sandy bottom after trawling disturbance. Lee et al. (2001b)
found that copepods in a shallow Antarctic bay were among the first
organisms to recolonize the fresh scour. Since our experimental set up
consisted of a closed microcosm, we could not observe any recolonization
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Chapter VI. Sedimentation and selectivity experiments
process. Therefore the interpretation of this drop in abundances for the
surface harpacticoids would need further investigations.
Next to the effects of sediment displacement on the meiobenthic
assemblage, we were interested in the potential responses of the
meiobenthic assemblage to three different types of detritus (benthic
microalgae, phytoplanktonic haptophyte and macroalgae) after the
disturbance.The likely increase of macroalgal biomass production in the
inner part of Potter Cove as a result of the newly available rocky areas that
arise from beneath the retreating glacier (Quartino et al., 2013) could
represent an important energy source for benthic assemblages.
Macroalgae can be directly consumed by herbivores (e.g. amphipods) or
indirectly by bacterivorous metazoans (e.g. some nematodes and
harpacticoid copepods taxa) feeding on the surface bacterial associations
(biofilm) on healthy thalli (Bengtsson et al., 2011) or on the fragmented algal
detritus (Buovy et al., 1986; Kristensen and Mikkelsen, 2003; Reichardt and
Dieckmann, 1985). Another newly available source of food in the changing
Antarctic marine environment will be that resulting from the sedimentation of
smaller soft cells phytoplanktonic microalgae as a consequence of the
climate-change driven shifts in the dominant phytoplankton community size
classes (Moline et al. 2004; Hernando et al., unpubl. data). In fact
organisms that are not adapted to break the hard diatom shells could
exploit this more accessible freshly produced primary production. From our
experiment there is no evidence that different types of detritus would have a
significant effect on the meiofauna community in terms of densities and/or
diversity within the temporal framework of the experiment (2 weeks).
Nevertheless, the lowest densities were recorded in the macroalgae and
Iscohrysis galbana treatments. On the other hand, the nematode
assemblage seemed to respond with changes in the relative abundances of
the different trophic guilds between the treatments. Epistrate feeders (2A)
remained the most abundant trophic guild in both the control and the
Seminavis robusta treatments, and in these samples the nematode
assemblage resembled the most to the in situ assemblage, with
Dichromadora representing more than 20% of the assemblage.
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Chapter VI. Sedimentation and selectivity experiments
Table 2 Nematode genera average relative abundances (%, 0-2 cm layer) for the natural sediments (Natural) and for the four
treatments of the "food selectivity" experiment after 1 week incubation time.
Natural
%
Control
%
Macroalgae Det
%
Isochrisys galbana
%
Seminavis robusta
%
Dichromadora
22.83
Dichromadora
29.88
Sabatieria
22.30
Dichromadora
16.80
Dichromadora
24.75
Daptonema
17.57
Aponema
15.58
Aponema
15.39
Aponema
14.36
Aponema
17.82
Chromadorina
13.22
Daptonema
9.30
Dichromadora
10.49
Sabatieria
12.21
Daptonema
12.87
Spiliphera
9.19
Sabatieria
7.70
Daptonema
7.50
Chromadorina
10.68
Sabatieria
6.93
Chromadorita
4.71
Chromadorina
5.62
Desmolaimus
5.99
Daptonema
10.61
Desmolaimus
5.94
Aponema
4.03
Linhomoeus
4.96
Chromadorina
4.96
Metalinhomoeus
6.24
Marylynnia
4.95
Eleutherolaimus
3.67
Metasphaerolaimus
4.83
Marylynnia
4.96
Southernia
5.91
Amphimonhystrella
2.97
Stylotheristus
2.83
Camacolaimus
2.83
Metasphaerolaimus
4.49
Metasphaerolaimus
3.69
Leptolaimus
2.97
Desmolaimus
2.60
Paracanthonchus
2.66
Linhomoeus
4.46
Ascolaimus
2.16
Acantholaimus
1.98
Leptolaimus
1.88
Molgolaimus
2.21
Odontophoroides
2.94
Halomonhystera
1.53
Chromadorina
1.98
Parachromadorita
1.72
Leptolaimus
1.72
Southerniella
2.50
Leptolaimus
1.53
Innocuonema
1.98
Odontophoroides
1.66
Odontophoroides
1.72
Amphimonhystrella
1.52
Linhomoeus
1.53
Linhomoeus
1.98
Southerniella
1.66
Eumorpholaimus
1.68
Chromadorita
1.52
Paracanthonchus
1.53
Metasphaerolaimus
1.98
Linhomoeus
1.43
Metalinhomoeus
1.15
Ascolaimus
1.49
Prochromadorella
1.53
Odontophoroides
1.98
Sabatieria
1.30
Cyatholaimus
1.11
Paramonhystera
1.49
Desmolaimus
1.25
Theristus
1.98
Marylynnia
1.07
Chromadorita
1.06
Leptolaimus
1.01
Halalaimus
1.14
Chromadorita
0.99
Prochromadorella
1.07
Araeolaimus
0.57
Halalaimus
1.00
Paramonhystera
1.14
Prooncholaimus
1.07
Eleutherolaimus
1.02
Southernia
0.88
Atrochromadora
0.63
171
Chapter VI. Sedimentation and selectivity experiments
Dichromadora is a genus belonging to the Chromadoridae, a family
characterised by a large number of epistrate algae feeding nematode
genera (Schiemer, 1987). In Potter Cove microphytobenthos is expected to
be one of the most important food sources given the usually low
phytoplanktonic primary production of the inner cove (Schloss et al., 2002;
Schloss et al., 2012), and the dominance of nematode epistrate feeders in
the cove sediments have been previously reported (Pasotti et al., 2012,
2014a). The shredded macroalgae detritus and the likely more easily
degradable haptophyte detritus lead to a nematode assemblage dominated
by non-selective deposit feeders (1B), followed closely by epistrate feeders
(2A). The nematodes belonging to the 1B feeding group ingest in a nonselective way food particles such as large bacteria and diatom cells. Their
buccal cavity is only weakly cuticularized and it is plausible that they benefit
from the soft-celled detritus added to the sediments. The fragmentation of
the macroalge detritus enhanced the total surface that can be colonised by
the bacteria (Buovy et al., 1986; Kristensen and Mikkelsen, 2003), which
may have favoured those nematodes capable of feeding on the biofilm.
Where bacteria degradation of macroalgae takes place, oxygen may
become limiting and toxic waste products (such as H2S) can be released in
the sediment. The higher abundance of Sabatieria (22.30%) in the
macroalgae treatments may support this inference. Sabatieria is known to
be a genus capable of thriving in low oxygen conditions (Wetzel et al. 2002)
and is usually living in the deeper layers. The higher relative abundance of
this genus and the overall lower meiofauna densities found in the
macroalgae samples may point at possibly less favourable oxygen
conditions in these units.
6.
Conclusions
The outcome of these two experiments shows that the surface meiobenthic
assemblages of Potter Cove shallow water is highly adapted to heavy
sudden loads of inorganic sediment and to possible abrupt displacements.
In fact the distribution within the sediment of the most abundant taxon
(nematodes) is not impacted by such events, but more likely other factors
may be involved (e.g. organic matter availability, predation and other form
of physical disturbance such as ice scour and re-suspension). Copepods
were the most sensitive group to the sediment displacement, although their
potential avoidance of the event (by rapidly swimming away during the
sediment collection) cannot be excluded. Different detritus types did not
impact the overall abundances of the nematodes but seemed to have an
effect on the nematode trophic guild composition after one week of
incubation, with macroalgae and small soft-celled haptophyte detritus
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Chapter VI. Sedimentation and selectivity experiments
favouring (attracting?) non selective deposit feeders (1B) whereas control
samples and benthic diatom detritus treatment showed the higher
dominance of epistrate feeders (2A). Further investigations with relation to in
situ conditions can shed more light on the factors that affect meiofauna
vertical distribution and trophic composition of nematodes in Potter Cove.
7.
Aknowledgements
We acknowledge the ESF IMCOAST project (Impact of climate induced
glacial melting on marine coastal systems in the Western Antarctic
Peninsula region, www.imcoast.org) within which this work was carried out.
The first author was financed through an IWT PhD scholarship and by Ghent
University at the time the experiments were carried out and processed. We
would like to thank the Alfred Wegener Institute (AWI, Germany) and the
Instituto Antartico Argentino (IAA, Argentina) for the logistics at Dallmann
laboratory in Carlini station (former Jubany). We would like to thank AWI
divers for the diving logistics. Special thanks go to Oscar Gonzáles for his
assistance and logistic support. Lastly, we would like to thank Marcelo
Hernando (National University of La Plata, Argentina) for the culturing of the
phytoplanktonic diatom species that was added to one of the experiments.
173
Chapter VII. General discussion
Penguin Rookery – Phygoscelis papua
“I am hopeful that Antarctica in its symbolic robe of white will shine forth as
a continent of peace as nations working together there in the cause of
science set an example of international cooperation.”
Richard E. Byrd
Explorer
(1888-1957)
Chapter VII. General discussion
1.
Key findings
The primary objective of this thesis was to investigate Potter Cove benthos
responses to local glacier retreat, while also generating a sound baseline
for future studies. Key findings include:







The data obtained in the current study, agreeing with the previous
literature, indicate that Potter Cove’s shallow benthos is
responding to in situ glacial retreat with structural (biomass and
taxonomic composition) and functional (isotopic niche width)
changes, and that meiofaunal organisms appear to be a more
resilient size class than macrofauna.
Glacier-retreat-related impacts on the biological communities
depend on the organism turnover rates (recruitment potential),
dispersal potential (capacity of re-colonisation or local migration),
motility (behavioural avoidance of ice scour impact) and dietary
flexibility (resilience to overall disturbance).
Ice scour and wind-driven re-suspension are very important
disturbance factors, with both “positive” and “negative” effects on
the benthos. Increases in their frequency are likely to be
detrimental to most macrobenthic species, and to have overall
strong influences (but not catastrophic) for the highly detritus
based meiobenthic assemblage.
Meiofauna represent a pioneer size class for newly ice-free, heavily
scoured soft bottoms, where wave-driven re-suspension is lower.
Macrofauna are poorer competitors at high disturbance levels, but
increase in dominance at intermediate and low disturbance levels.
In the latter circumstances, competition for resources between
meiofauna and macrofauna may become more important in
shaping community structure and the food web.
The meiofauna, being trophically connected to both detritus and
microorganisms, and to macrofauna, display a higher resilience to
disturbance in light of an intrinsic size-dependent centrality in the
overall benthic food web and the high trophic redundancy present
in important contributing taxa (e.g. nematodes).
Inorganic sedimentation does not affect meiofauna abundances.
Nematodes and copepods, in particular, seem resilient to this
source of disturbance. Fresh detritus may have positive effects on
their abundance.
Food quality changes (increase in macroalgal detritus and more
accessible soft-celled phytoplankton flagellates) can stimulate
bacterial degradation within the sediment and initiate short-term
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Chapter VII. General discussion

community shifts in the nematofauna, with genera such as
Sabatieria or Halalaimus becoming more abundant. Abundances
can be temporally negatively affected, especially those of oxygen
sensitive taxa (e.g. harpacticoid copepods).
Ice scour seems to have a negative effect on the relative
abundance of selective feeding nematode.
In this chapter I provide an overview and synthesis of these key findings in
relation to the questions posed originally in Chapter 1 and the wider
literature (Section 2). I make general considerations on benthic community
dynamics in the context of climate change (Section 3; Fig. 1, 2). Finally, I
provide brief comments on the methodologies used and possible
improvements, and recommendations for future research (Section 3).
2.
Potter Cove shallow benthos and recent rapid glacier retreat: main
insights from a two-fold investigation
Antarctic biological communities have been (and still are) shaped by
different drivers acting on millennial (e.g. continental ice sheets waxing and
waning between glacial maxima and interglacial periods) to yearly-decadal
(e.g. El Niňo Southern Oscillation, ENSO) time scales (Barnes and Conlan,
2007). Ice scouring, high winds, hypoxia, volcanism, localised pollution and
ultraviolet (UV) radiation are amongst the disturbances that Antarctic
organisms have adapted to and which at present they experience daily
(Barnes and Conlan, 2007; Convey et al., 2009c). It seems legitimate to
wonder what may realistically represent a disturbance for such “extreme”
biological communities.
Potter Cove (PC) is situated on the southern shore of King George Island
(Isla 25 de Mayo, South Shetland Islands), an island with a small ice cap
which drains to several coastal inlets. PC is one of three tributary fjords of
Maxwell Bay (see Fig. 6 Chapter I, Introduction). Since the end of the Little
Ice Age (LIA) cold period (1400-1850/1900 A.D.), sediment accumulation
rates in Maxwell Bay have increased (Hass et al., 2010) and, since the
1930s, the rates have tripled as a consequence of the rapid regional
warming (RRW) trend observed in recent decades (Monien et al., 2011).
The Fourcade glacier (PC tidewater glacier) terminus is estimated to have
been located at the head of the fjord at the end of the LIA (Hass et al.,
2010), and to have been in retreat since, with an average retreat rate of
about 30 m year-1. A rapid increase in retreat has taken place since the
1930s (Monien et al., 2011), as a consequence of glacier disintegration due
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Chapter VII. General discussion
to the up-lifting of the thinning ice by the intrusion of sea water. Today, the
glacier has almost completely retreated past the shoreline (Rückamp et al.,
2011).
Large concentrations of brash ice, floating ice and ice growlers dominate
the cove’s summer landscape, and sediment-laden melt waters are
discharged during summer by glacial riverine systems. New benthic icefree areas have asynchronously appeared within the past 20 years from
beneath the ice of the inner part of the fjord (Rückamp et al., 2011). The
rocky shores of these newly ice-free sites has been colonised by seaweeds,
enhancing local primary production (Quartino et al., 2013). The summer
glacial melt water discharge causes freshening of the surface waters in the
inner cove, with consequences for the water column stability and turbidity.
Phytoplankton community shifts have been reported in this area, with
decreases in the relative abundance of the common dominant larger
diatoms and increases in the contribution of small phytoflagellates, linked to
the local freshening events (García et al., under review), as has previously
been documented for other Antarctic locations (Moline et al., 2004). In the
western Antarctic Peninsula (WAP) region Montes-Hugo et al. (2009)
reported an increase in wind speed of about +60% since the 1970s. At
Rothera station (Adelaide Island, 68°S) Barnes and Souster (2011)
documented a decrease in fast ice (also called land-fast ice, a form of
winter sea surface ice which can lock in icebergs and prevent wave action)
duration of 5 days year-1 over 25 years, which was correlated with increases
in ice scour frequency and reduced benthos survival. Similarly, in the inner
part of PC high bed shear stress on exposed shallow sites was recently
documented (Wölfl et al., 2014) and ice scour impact represents one of
seasonal disturbances.
The sediment communities developing in the inner part of PC have been
exposed to the consequences of local glacier retreat over the last few
decades. Recently previously ice-covered areas have faced sudden
exposure to open water dynamics (e.g. bed shear stress through wave
action caused by strong winds), with the duration of these influences
varying due to their asynchronous exposure. The recent and ongoing
changes in food source quality and quantity, increased inorganic
sedimentation and re-suspension, increase in ice scour frequency and the
appearance of newly ice-free open water areas in the inner part of the fjord,
are all events which are expected to influence the benthos via complex
interactions and ecological feedbacks.
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Chapter VII. General discussion
The synergies between different climate change-related changes may have
both positive and negative effects on shallow water benthic assemblages.
These effects manifest in a (dynamic) mosaic of assemblage structures and
trophic organisations within a spatially restricted area, in light of the spatial
heterogeneity that disturbances are known to create (Gutt and Piepenburg,
2003; Sousa, 2003; White and Jentsch, 2001 and references therein). As
outlined in Chapters II and III, the appearance of new ice-free sites seems
to represent a positive outcome of glacier retreat, as it makes available
important space and trophic niche resources that the different benthic size
classes can exploit. Small-sized meiobenthic organisms were pioneer
colonisers, showing rather diverse, abundant assemblages and wide
isotopic niches at the most recently ice-free and disturbed study site.
Copepod recruitment appeared to be favoured in early summer while, for
the most abundant taxon (the nematodes), adults/juvenile ratio did not
change between seasons. These observations are consistent with the
findings of the laboratory studies described in Chapters V and VI. During
these short-term laboratory experiments, the abundant nematodes were
demonstrated to be highly resistant to imposed sediment loads and abrupt
substrate displacement, with only minimal losses in abundance and taxa
diversity, while copepods and nauplii were the most affected groups.
Additionally, the three most important meiofaunal organisms (nematodes,
copepods and cumaceans) were highly flexible in their feeding
preferences, taking up carbon from both phytoplankton and bacterial food
sources, although in small amounts, while the nematofauna were very
capable of adapting to different types of detritus, with variations in the
relative abundance of specific feeding strategies.
PC soft-bottom macrofauna were poorer competitors than meiofauna for the
newly available space. Where ice scour and glacial melt water disturbance
was higher, small, mobile higher trophic level consumers or other pioneer
species established, whereas sessile forms (e.g. the sea pen
Malacobelemnon daytoni) appeared to be absent. The macrobenthic
assemblages at the highly disturbed sites (Isla D and Creek) showed low,
scattered (patchy) abundances and biomasses, dominated by scavengers
and predators that were likely benefitting from the dead material generated
by repeated ice scour impacts. In contrast, at the low disturbance site
(Faro), the assemblage was characterised by a more complex, less patchy
but abundant fauna. Under this level of disturbance sessile filter feeders (M.
daytoni) were present together with older individuals of Yoldia eightsi (a
suspension-feeding bivalve). The food web was characterised by strong
benthic-pelagic coupling, tightly linked to a detritus-based “small food web”
(the meiofauna), resulting in better overall stability.
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Chapter VII. General discussion
The selective/structuring force exerted by ice scouring has been previously
described in detail for Adelaide Island (WAP) shallow benthos by Brown et
al. (2004) and Smale (2008), and in Potter Cove by Sahade et al. (1998).
The epifaunal communities here, as in other Antarctic locations, presented a
strong bathymetric profile with increasing abundance, biomass and
diversity with increasing depth, resulting from reduced ice disturbance with
increasing water depth (Brown et al., 2004; reviewed by Gutt, 2001; Sahade
et al., 1998; Smale, 2008). Community shifts have been reported (and are
still occurring) in the inner part of glacial fjords such as Potter Cove
(Sahade et al., 1998). Ice scour disturbance has been identified as the main
driver of the high benthic diversity of the Antarctic shelf, whilst low levels of
melt water discharge have been linked to the higher biodiversity found in
Antarctic fjords (Barnes and Souster, 2011; Grange and Smith, 2013; Gutt,
2001). Where ice disturbance is low, biological competition becomes the
main driver of species diversity, and communities may become dominated
by single k-strategist species (Barnes, 2002).
The Antarctic is known for the highly hierarchical character of competition,
with lower competitors failing more often, risking local extinction (Barnes,
2002), resulting in an overall regional decrease in diversity. However,
recently Barnes and Souster (2011) observed that a decrease in fast-ice of
5 days year-1 over the past 25 years was positively correlated to an increase
in ice scour frequency above previous natural levels, and this was related to
a higher mortality of the common bryozoan species Fenestrulina rugula.
They argued that the observed (and predicted in future) increases in the
frequency of iceberg impact due to WAP climate change would lead to
reduced survival of shallow ecosystem benthos. However, it is also
appropriate to note that this conclusion was based on the survival potential
of one of the most common sessile shallow bryozoan species and one sizeclass of organisms (macroepibenthos). It is also possible that mobile
organisms, such as omnivorous scavengers (e.g. polynoid polychaetes),
active swimmers (e.g. cumaceans) or burrowers (e.g. the bivalve Laternula
elliptica) may be capable of avoiding some of the impacts of ice scour,
thereby becoming potential winning organisms at shallow depths.
In light of their different size spectra, recruitment/dispersal potential and the
different fractal dimension of their environment (the smaller the size, the
higher the number of available “spatial niches” per disturbed area
(Woodward et al., 2005)), meiofaunal organisms may not respond in the
same fashion to ice disturbance as the larger macro- and megabenthic
Antarctic metazoans. In the current study, the soft bottom macrobenthic
assemblage at the less disturbed site was distinctly characterised by the
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Chapter VII. General discussion
presence of the pioneer sessile pennatulid M. daytoni, which was absent at
the other two study locations at the same depth. This opportunistic (annual
life cycle) species was previously reported as highly dominant on the soft
bottoms of the inner cove in the vicinity of our melt water dischargeinfluenced site (Sahade et al., 1998b). The absence of pennatulids at the
highly disturbed creek site during our study may be the result of (i) their low
recruitment due to ice scouring (and hence under sampling by means of
van Veen grab) or (ii) the effect of the recent increase in overall disturbance
(e.g. increase ice scour frequency, melt water run-off and bed shear stress)
above a threshold limit which this usually opportunistic species failed to
survive. At this location, instead, mobile polynoid scavengers and younger
individuals of Y. eightsi dominated the macrofauna. The bivalve Y. eightsi is
known for being a shallow burrower capable of feeding while totally buried
(Davenport, 1988), an ability which may enhance its resilience (defined as
“… the capacity of an ecosystem to absorb disturbance without shifting to
an alternative state and losing function and services”, Côté and Darling
(2010), and references therein), under high sediment laden melt-water
discharge. The high biomasses of mobile scavenger polychaetes found at
both highly disturbed sites could be a result of their motility and low dietary
specialisation, as reported for Mediterranean land communities where
survival in response to fire was found to be significantly higher for mobile
non-selective feeding organisms (Santos et al., 2014).
The maintaining of the different successional stages observed in the three
investigated assemblages, and the increase in complexity with time since
ice retreat, are consistent with the conclusions of studies on Antarctic
terrestrial vegetation (Convey & Smith, 2006; Favero-Longo et al., 2012),
invertebrates (Gryziak, 2009) and nematodes (Ileva-Makulec Krassimira
and Grzegorz, 2009), benthic macroalgae (Quartino et al., 2013), intertidal
communities (Pugh & Davenport, 1997) and benthic communities formed
after-ice shelf collapse (Gutt et al., 2013; Raes et al., 2010). In all these
studies the complexity and diversity of assemblages at the newly-exposed
sites was positively correlated to the time since ice retreat, relating to the
growing availability of food resources and the sequential arrival of direct
and indirect consumers. In Potter Cove, newly-exposed rocky shores are
undergoing seaweed colonisation and local primary production is therefore
bound to increase (Quartino et al., 2013), with consequences for benthic
deposit feeders and non-selective filter feeders (e.g. the ascidian
Cnemidocarpa verrucosa; Tatián et al., 2004). Nevertheless, from the
evidence presented here in Chapter VI, macroalgal detritus can have
(temporary) negative effects on meiobenthic standing stock and also can
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Chapter VII. General discussion
initiate community shifts in the nematode assemblage, favouring bacteriafeeding and low oxygen-resistant genera.
Colonisation (and subsequent succession) of the associated soft-bottom
ice-free space by benthic organisms is likely to be a continuous process
working on temporal scales that are dependent on the organisms’
synecology and their resilience to ice scouring and other glacial
disturbances. Slow recovery times are the norm for megaepibenthic fauna
in such extreme environments (Brown et al., 2004), although adaptation to
disturbance may have evolved in certain groups and the recovery rates
may vary among different taxa (Smale et al., 2008a). Colonisation by smaller
meiobenthic organisms can happen via active or passive relocation in the
water column (Palmer, 1988). Potter Cove, as with many other Antarctic
marine ecosystems, is a high energy environment where wave action can
re-suspend sediment down to at least 30 m depth. Lundquist et al. (2006)
observed that meiobenthic re-colonisation was favoured by site
hydrodynamics, and the relative buoyancy and life-history strategy of the
coloniser organisms. The high turnover rates and floatability of meiobenthic
metazoans are features that facilitate their return to scoured sediments from
both neighbouring and distant un-scoured patches, permitting rapid reestablishment of high densities (Lee et al., 2001b). Furthermore, the high
trophic flexibility of the most abundant taxon (the nematodes) and its
assemblage’s inherently high functional redundancy (different nematode
genera/species can feed on the same range/type of resources) is a very
important feature in ensuring resilience under changing environmental
conditions (White and Jentsch, 2001). In Potter Cove, nematodes and
copepods appeared to be the most rapid colonisers of newly available
substrata. In general, the meiofauna, being connected both to the detritus
and microorganisms and the macrofauna, display a higher resilience to
disturbance in the light of the intrinsic size-dependent centrality in the
overall benthic food web (Woodward et al., 2005).
Similar higher resilience and faster recovery of meiofauna when compared
to macrofauna, observed during this investigation, was also reported by
Peck et al. (1999) in the sub-Antarctic after a catastrophic iceberg scouring
event. The higher turn-over, direct connection with the detrital-microbial
pool and specific taxon-related life history strategies may facilitate earlier
colonisation by these small organisms. Global climate change models
applied to pelagic communities also predicted higher resilience in the
small-size component of the community, relating it to both their lower
metabolic requirements and the overall lower predatory pressure in light of
the decline of larger organisms (Lefort et al., 2014). Nematodes are known
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Chapter VII. General discussion
to be highly flexible in terms of their trophic preferences. The nematofauna
at the most disturbed study site showed community differences that
highlight different successional stages and are a sign of trophic
adjustments at the community level. The dominant genera were
Microlaimus, which is known to be a rapid coloniser of iceberg scours (Lee
et al., 2001b) and Daptonema, a highly “plastic” genus, capable of feeding
on both microalgae and bacteria (Vanhove et al., 2000). The other two study
locations hosted much more similar nematofauna assemblages in terms of
the most representative genera, pointing at ongoing community shifts at the
three sites in response to their relative newly ice-free status and the
continuing summer ice scour disturbance. There was also a notable
decrease in the relative abundance of selective deposit-feeders (bacteria
feeders, trophic guild 1A), from around 30% in winter and early summer
(Chapter IV) to ≤ 10% later in summer (Chapter II). Such a negative effect of
summer ice scouring (or, alternatively, a higher importance of bacterialderived detritus during winter ice scour-free periods) on the relative
abundance of nematode selective deposit feeders was previously reported
for Weddell Sea shelf nematode communities (Lee et al., 2001a).
Warwick (1988) and Heip et al. (1988) stated that the short generation time
and the lack of a dispersal phase of many meiofaunal organisms, interalia
including nematodes, would make these small-sized metazoans more likely
to be affected by rapid changes than the larger macrofauna. Meiofaunal
organisms can indeed respond quickly to disturbances with changes in the
assemblage structure, but this does not automatically imply permanent
consequences for the community. Many disturbances are short-lived and,
for instance, the most abundant taxon within the meiobenthos, the
nematodes, seem to be strongly affected by types (frequency and degree)
of disturbance they do not experience naturally (Schratzberger et al., 1999).
In the WAP ice scour impact is a common feature and the recent increase in
its frequency as a result of the climate change-driven reduction in fast ice
duration (Barnes and Souster, 2011) currently remains within the natural
variability of the system (Thomas et al., 2013). In the future, anthropogenic
climate drivers are expected to increase in influence on Antarctic climatic
trends, and more extreme changes are likely to take place. In Potter Cove
the next decade is likely to see the complete retreat of the Fourcade glacier
front onto land, with an associated rapid reduction in ice scouring of the
inner cove shallow benthos. Additionally, if the increase in air temperatures
and ice mass loss on King George Island continue, this may ultimately
result in less melt water discharge into the cove, again resulting in an
overall reduction in the disturbance level the benthic communities will
experience.
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Chapter VII. General discussion
Disturbance was defined by White and Pickett (1985) as “any relatively
discrete event in time that disrupts ecosystem, community or population
structure and changes resources, substrate availability or the physical
environment”. Wayne Sousa, a key expert in biological responses to
ecosystem disturbances, defined it as “…a discrete, punctuated killing,
displacement, or damaging of one or more individuals (or colonies) that
directly or indirectly creates an opportunity for new individuals (or colonies)
to become established” (Sousa 1985, p. 356). The frequent catastrophic
disturbance of ice scouring outweighs biological interactions in the
structuring of shallow benthic communities and it is at the base of the
maintenance of habitat heterogeneity and biological diversity at the regional
(> 100 m2) scale (Barnes, 2002; Gutt and Piepenburg, 2003). In the
absence of ice scouring and high wind driven disturbance, Antarctic
benthic communities would be characterised by assemblages dominated
by a very small number of K-strategist species which would likely
monopolise space, outcompeting all other lower competitors (Barnes, 2002;
Barnes and Souster, 2011). Such biological outcomes from environmental
disturbances have been reported previously for temperate stream algal
assemblages (Ledger et al., 2008), marine intertidal boulder field benthic
assemblages (Sousa, 2003) and marine epifaunal communities (Osman,
2014). This pattern is indicated in the current study by the presence on a
regional scale (≥ 1 km2, Gutt and Piepenburg, 2003) of different benthic
communities with various life history strategies at the same water depth.
3.
General considerations and conclusions
In analysing possible responses of biological systems to climate-induced
perturbations of natural conditions, two separated processes that form the
concept of resilience have to be considered: the resistance – or the
magnitude of disturbance that affects the assemblages - and the recovery –
the time needed to return to pre-disturbance conditions (Carpenter et al.,
2014; Côté and Darling, 2010). Usually resilience was thought to be higher
in undisturbed, diverse and highly redundant communities compared to
degraded ones (Peterson et al., 1998). Nevertheless, Côté and Darling
(2010) have recently challenged this view and shown, for human-disturbed
coral ecosystems, how biodiversity and resilience are not directly related.
Rather, they argued that disturbed coral assemblages appeared to be more
resilient (resistant) to climatic changes since human-induced disturbance
already selected for disturbance-resistant species. Nevertheless, they also
added that, when recovery was addressed, more diverse coral
assemblages recovered faster than degraded ones.
182
Chapter VII. General discussion
Fig. 1. Scheme
summarising the main
drivers and trends of
benthic community
structure in Potter Cove.
Benthic community
dynamics are
schematised as the
variation in species/taxa
numbers through
different ecosystem
states (Y-axis) over time
(X-axis), the latter being a
dynamic, sequential
evolution of various
climate change-related
environmental stressors.
Abbreviations: LIA =
Little Ice Age; ENSO = El
Niño-Southern
Oscillation; TPA =
Tropical Pacific
Anomalies; SAM =
Southern Annular Mode;
r- and K- strat. = r- and
K- strategists; f =
frequency; Inorg. Sed. =
inorganic sedimentation.
183
Chapter VII. General discussion
A schematic resume of possible ongoing and future climate-related
environmental changes and linked responses of the Potter Cove benthos is
presented in Fig. 1, and may be extrapolated to other shallow water
Antarctic fjord communities. The initial environmental heterogeneity created
by disturbance increases Antarctic benthic assemblage diversity on a
regional scale until an intensity threshold is reached. This threshold relates
to climate change-induced anomalies. Once the degree of disturbance
exceeds that experienced in the natural regime and the threshold is
passed, local extinction is likely to take place. Those species that were
relatively widespread and abundant in the shallow depths (to 20 m in PC) to
this point, will be challenged by their synecological limits to (i) survive the
large gradient of the environmental change, while (ii) succeeding in the
struggle for space against the other competitors, and will likely migrate
and/or become locally extinct. This will result in a general decrease in
species/taxa diversity, as foreseen by Barnes and Souster (2011), with nonstochastic selection at shallow depths towards more disturbancetolerant/opportunistic r-strategist species. In turn, this will increase the
overall assemblage resilience (ability to resist the impacts of climate
disturbance) to further changes (Côté and Darling, 2010). At a later stage,
the glacial disturbance will largely cease, after the glacier retreats
completely on to land and glacial melt water discharge drastically
diminishes in light of ice mass loss. Hence the shallow habitats will become
mostly influenced by wind-driven disturbance. Climate models predict
increases in wind speed and wave height beyond the present (and past)
natural variability (Dobrynin et al., 2012; Eichelberger et al., 2008) and,
combined with the observed reduction in fast ice (Barnes and Souster,
2011), this will expose the shallow AP benthos for longer periods to winddriven mechanical direct re-suspension and indirect boulder destruction.
To date almost nothing is known about possible direct effects of wave
action and storm surge on Antarctic benthic communities. However, wave
action has usually been considered a much lesser structuring force on the
benthos compared to ice disturbance. Therefore, if wave action is
considered as a negligible structuring force and, rather, as a means for
species re-distribution, PC shallow marine habitats will become more
homogeneous in terms of disturbance once glacial activity has ceased.
Finally, those species surviving the initial period of increased disturbance
by migrating to nearby refugia (e.g. the inner deeper waters or sheltered
areas of the outer cove), will probably re-colonise the shallow areas, with
more effective competitors soon monopolising the available space (Fig. 1).
If biological competition becomes the main driver of benthic diversity, fjord
ecosystems like PC will probably face a general loss in biodiversity and
184
Chapter VII. General discussion
likely develop towards a lower resistance and slow recovery ecosystem
state.
Nevertheless, differences at the size spectrum level in the possible
responses of the benthos need to be considered (Fig. 2). Combining the
evidence obtained in the current study and the available literature, it is likely
that meiofaunal and macrofaunal organisms will display (and have
previously displayed) very different resilience to past, ongoing and future
scenarios. The meiobenthic assemblage seems highly resistant to
contemporary changes, and in light of their short generation time, feeding
plasticity and within-taxon high functional redundancy, the overall resilience
of the community, and hence its stability, might be expected to remain
relatively unchanged in the longer term.
In contrast, the highly hierarchical competition that characterises the
macrobenthos at low disturbance levels and the consequent potential
monopolisation of space by single species is likely to generate a low
redundancy-low stability assemblage in the Cove, which may affect its
resilience to further future environmental changes.
185
Chapter VII. General discussion
Fig. 2. Benthic
community resilience
(resistance - darker
coloured lines - and
recovery – lighter
coloured lines)
dynamics for meiofauna
(red/orange) and
macro/megafauna
(black/grey) through
different ecosystem
statuses (Y-axis) over
time (X-axis), the latter
being a dynamic,
sequential evolution of
various climate changerelated environmental
stressors.
Abbreviations: LIA =
Little Ice Age; f =
frequency ; Inorg. Sed.
= inorganic
sedimentation.
186
Chapter VII. General discussion
4.
Methodological improvements and future directions
By focusing on three contrasting study sites (with different glacier retreatrelated history), coupled with the in situ study of different size classes of
organisms (meio- and macrofauna), characterised by different turnover
rates, feeding strategies and dispersal potential, this study can make
inferences on the historical influences of glacier retreat on the resident
benthic communities and detect possible size-related biological responses
(Chapters II and III). The analysis of the effects of distinct potential glacialrelated environmental stressors on PC meiobenthos by means of laboratory
experiments (Chapters V and VI) and the in-time analysis (Chapter IV) of the
in situ meiofauna standing stocks, provided further evidence aiding the
interpretation of the main findings from Chapters II and III. Although the
small-scale laboratory experiments performed have a limited capacity to
allow generalisation about meiobenthic responses in the field, as there are
clearly intrinsic limitations in replicating the complex natural environmental
conditions in the laboratory (Schratzberger et al., 2000), the results
obtained were generally consistent with the in situ observations reported in
this thesis and by other authors.
Nevertheless, to link unequivocally the in field observed patterns to aspects
of the well-documented rapid regional warming and other environmental
changes while at the same time ruling out natural variability, it will be
necessary to gather long-term data including information on variation in
meiofauna and endomacrobenthos at the three study sites. In this respect,
imminent campaigns (just completed January-March 2015 and future
November-March 2015/2016) within the vERSO project will replicate
elements of the current study on meio- and endo-macrofauna at the three
study sites, and will also include in situ measurement of nutrient fluxes and
benthic respiration. This will provide additional information concerning the
functional responses to local environmental changes of the three benthic
assemblages in Potter Cove and their overall contribution to the cove’s
energy fluxes. Furthermore, replicating these studies in other areas,,
thereby increasing the scale of the analysis, is of fundamental importance.
Comparing areas with (i) similar (fjord-like embayment with glacial activity)
and/or (ii) different (no effect of glacier retreat, higher influence of anchor
ice) conditions will allow (i) confirmation of the observed patterns, and (ii)
help refine interpretations. Therefore, within the framework of the vERSO
project and related studies, investigation of the soft bottom meiofauna and
endomacrobenthos of the Kerguelen Islands and Terre Adélie are planned.
The Kerguelen Islands are a group of sub-Antarctic islands in the Indian
Ocean which remain ice-free all year around, and where land-based
187
Chapter VII. General discussion
glaciers are present. Terre Adélie is located in East Antarctica, and is an
area highly influenced by sea ice extent. Several tidewater glaciers are
present and, also influenced by sea ice dynamics, produce icebergs that
can scour the local benthos. Anchor ice constitutes a typical feature in this
high Antarctic region. These two locations present both similarities and
contrasts compared to Potter Cove, and the investigation of their benthic
communities and food webs, integrating the results with the current study,
will provide a great opportunity with which to interpret and model the likely
responses of Antarctic and sub-Antarctic organisms to regional climaterelated dynamics. Finally, an historical (1999) unprocessed collection
(belonging to the Alfred Wegener Institute, Germany) of Potter Cove
sediment samples will be processed by the UGent for macrofaunal analysis
and comparison of higher taxa diversity will be used to infer on general
patterns of change in community structure and functional traits. This will be
coupled to recently sampled material for both meiofauna and macrofauna in
PC at the three investigated sites. This will become part of an extensive and
exciting dataset documenting meiofaunal abundance over a time frame of
two decades in Potter Cove, increasing depth in our understanding of
natural community fluctuations of these small-sized benthic metazoans.
With the continuous increase of CO2 and other greenhouse gases
atmospheric concentration, the Oceans are undergoing significant
acidification and predictions point to a drop in pH of up to -0.3 units by
2100 (IS92a scenario, IPCC 2007). Acidification events have been linked to
mass extinctions (Veron, 2008) during the Earth’s history and there is
growing concern that modern acidification is already effecting important
groups of the plankton (Arnold et al., 2009; Cummings et al., 2011; Dupont
et al., 2008). In the future investigations on the possible effects of
acidification on Potter Cove meio- and macrobenthic organisms is of
fundamental importance if we are to understand how this highly diverse
fjord-like ecosystem will be coping with the ongoing climatic changes.
Initially we want to investigate the sediment surface assemblage to see how
do they respond to short term increased acidification. We want to know
whether the ecosystem services provided by the benthos change due to
acidification. To answer to this we will investigate by means of a microcosm
laboratory experiment several aspects of the benthos:

Meiobenthic (included forams) assemblage diversity (higher taxa
surrogacy (Heino and Soininen, 2007) ) densities, biomass, trophic
composition and survival (forams shell damage – via electron
microscopy inspection - and nematode cell death – via DAPI cell
staining)
188
Chapter VII. General discussion





Macrobenthic assemblage diversity (higher taxa surrogacy)
densities, biomass, trophic composition, life traits analysis and
survival
Benthic respiration
These by means of incubations
Nutrients and carbon fluxes
Microbial abundance and diversity (ARISA, Sybr Green I/II staining)
Incorporation of different algal/bacterial food by adding fresh
macroalgae
detritus
versus
local
microbenthos
(both
microphytobenthos and bacteria) and tracing this food uptake by
means of specific natural biomarkers (the PolyUnsaturated Fatty
Acids - PUFAs)
189
Addendum
The “guardian friend” of Potter Cove: the Nunatak
“Antarctica: those are the eyelids that never close; this is the staring
unsleeping Eye of the earth; and what it watches is not our wars.”
Robinson Jeffers
Poet, ecological movement
(1887-1962)
Addendum
Table A1 Meiofauna (0-5 cm) abundance (n° ind. 10 cm-2) and biomass (µg C 10 cm-2).
Faro
Isla D
Creek
total meiofauna
1354 ± 603
3223 ± 1634
2918 ± 1384
Nematodes
1269 ± 576
3047 ± 1605
2862 ± 1387
Copepods
6±3
66 ± 33
13 ± 3
Cumaceans
5±6
0,5 ± 0,5
4,9 ± 7
651 ± 460
462 ± 290
1055 ± 182
8±6
73 ± 9
25 ± 8
21 ± 18
0
105 ± 113
Abudances
Biomass
Nematodes
Copepods
Cumaceans
190
Addendum
Table A2 Macrofauna biomass (mg AFDW m-2).
Creek
Yoldia eightsi
Mysella spp.
Genaxinus sp
Gasteropoda
Cirratulidae
Ophaelidae
Maldanidae
Spionidae
Orbinidae
Terebellidae
253
76
169
38
519
92
462
9819
42
72
48
475
Isla D
334
42
8
118
75
77
67
714
257
31464 41644
371
14
Polynoidae unidentified
Aglaophamus
trissophyllus
1188
175
142
239
53
36
497
38
178
34
147
66
90
235
4231
66
158
2317
Amphipodes
42
1638
546
22
42
54
482
119
20
499
Priapulus sp.
Malacobelemnon daytoni
2000
59
366
89
732
4155
1945
56
483
3198
76
3475
75
56
194
14
665
4333
4463
24
5472
887
232
14
496
740
56
14
282
3454
52
725
2626 4552
469
118
1320
268
45
229
46
233
889
74
238
Tanaidacea
Paraserolis polita
80
23
5253
546
15736
573
Oligochaetes
Eudorella sp.
Dyastilis sp.
Vauthompsonia sp.
414
73
98
2
2568
62
7789 7789 21252 11197 1834
786
Barrukia cristata
Faro
249
9
4768
6837
67
2336
24
1232
191
Addendum
Table A3. Macrofauna abundances (ind. m-2).
Yoldia eightsi
Mysella charcoti
Genaxinus sp
Gasteropoda
Cirratulidae
Ophaelidae
Maldanidae
Spionidae
Orbinidae
Terebellidae
260
43
998
130
130
87
Barrukia cristata
Polynoidae
Aglaophamus
trissophyllus
Other polychaetes
Oligochaetes
217
Eudorella sp.
Dyastilis sp.
Vauthompsonia sp.
1302
Amphipodes
Ostracoda
Tanaidacea
Paraserolis polita
Priapulus sp.
Malacobelemnon daytoni
434
1313
5611
358
119
Creek
239
239
239
478
119
478
119
239
Isla D
191
64
700
255
191
64
64
191
1015
1433
53
3236
298
119
382
637
716
60
220
424
159
212
637
2228
1433 1194
212
127
73
56
1791 1359
0
184
60
37
60
73
60
147
179
73
0
37
60
0
37
358
169
478
764
4457
255
64
5674
112
337
56
Faro
166
42
106
143
2076
0
457
5518
106
53
9073
143
382
48
56
64
64
225
106
191
56
96
1963 1910 5372 1873 2865 5857 19943 13079 13476 16522
318
0
716 624 637
53
0
119
265 147 298 220
255
393
83
424
239
48
382
64
700
225
506
42
208
53
212
143
191
955
192
Addendum
Table A4 Comparison of SIBER analysis results for the "complete dataset” analysis (left) and the "reduced dataset”
analysis (right) for the “by site” analysis.
By site analysis
complete dataset
reduced dataset
2
SEAc area (‰ )
Faro
19.88
19.88
Isla D
23.11
13.47
Creek
14.89
14.89
Bayesian posterior probabilities for SEAb by site (%)
Faro > Creek
90
90
Isla D > Creek
98
41
Isla D > Faro
84
9
SEAc Overlaps by site (‰2)
Faro and Creek
11.92
11.92
Isla D and Creek
6.19
0.0968
Isla D and Faro
9.15
1.96
193
Addendum
Table A5. Comparison of SIBER analysis results for the "complete dataset’ analysis (left) and the "reduced dataset” analysis
(right) for the “size by site” analysis.
Size by site analysis
complete dataset
reduced dataset
SEAc area (‰2)
Faro
Isla D
Creek
Faro
Isla D
Creek
Meiofauna
2.45
58.25
7.92
2.45
5.18
7.92
Smaller macrofauna
15.38
9.28
7.82
15.38
8.12
7.82
Bigger macrofauna
37.97
11.38
11.65
37.97
11.38
11.65
Bayesian posterior probabilitie for SEAb by site (%)
Faro
Isla D
Creek
Faro
Isla D
Creek
Meiofauna > Smaller macrofauna
0
100
64
0
71
56
Bigger macrofauna > smaller
macrofauna
99
99
90
99
95
88
Bigger macrofauna > meiofauna
100
1
71
100
33
75
194
Addendum
Table A6 Pairwise comparison between community wide metrics (Layman et al., 2007) for each site using Bayesian
posterior probabilities. Results are shown for both analysed datasets.
complete dataset
dNR
dCR
CD
MNND
SDNND
Creek > Faro
0.0433
0.9009
0.6181
0.4394
0.7622
Creek > Isla D
0.2704
0.5662
0.5184
0.3555
0.704
Faro > Isla D
0.7017
0.2384
0.4614
0.4169
0.5192
reduced dataset
Creek > Faro
0.046
0.9005
0.6329
0.45
0.7637
Creek > Isla D
0.01
0.1045
0.0138
0.0123
0.5956
Faro > Isla D
0.17
0.0208
0.0209
0.0598
0.3408
195
Addendum
Table A7 Chlorophyl-a and phaeopigments concentrations (µg g-1 dry weight sediment, average ± SD) and their
ratio for the two investigated sites during summer (SUM) and winter (WIN).
Chla
Phaeopigments
Phaeo/Chla
ST1
13.71 ±1.59
12.68 ± 3.81
0.92
ST2
63.01 ± 25.68
34.43 ± 12.06
0.55
ST1
6.64 ± 1.52
11.34 ± 1.1
1.71
ST2
8.66 ± 2.3
11.32 ± 2.25
1.31
SUM
WIN
196
Addendum
Fig. A1 Standard ellipse areas corrected for small samples size (SEA c, full lines) and
convex hul areas (dashedlines) for all sites (see legend) for the reduced dataset
analysis.
197
Addendum
Fig. A2 Standard ellipse area Bayesian estimations (SEAb) for the reduced dataset
analysis. Mode (black dots) and probability of data distribution (50% dark grey
boxes; 75% intermediate grey boxes; and 95% light grey boxes) for each site are
presented. The standard ellipse area corrected for small sample size (SEA c) is also
presented as red squares.
198
Addendum
Fig. A3 Standard ellipse area corrected for small sample size (SEA c) for each site
with the three consumer size classes (see legend for colors) from the reduced
dataset analysis.
199
Addendum
Fig. A4 Community wide metrics for the three sites (see legend for colors). The
dark squares are the mode, the triangles the Bayesian probability and the bars
represent the 95% credibility interval of the posterior probability distribution. NR =
Nitrogen range; CR= Carbon range; CD= mean distance from centroid; MNND=
mean nearest neighbour distance; SDMNND= standard deviation MNND.
200
Addendum
Fig. A5 Non-parametric Multidimensional scaling (nMDS) based on the
Richness “S” values of the meiofauna community during the SEL
experiment. Labels refer to Time (0, 1 week, 2 weeks). The legend
explains the treatments. Background = natural conditions at time 0. CTRL
= control treatment; MaDET= macroalga detritus; Dyno = Isochrysis
galbana detritus; MPB = microphytobenthos detritus.
201
References
My reference…my mentor…my friend…
”But why, it has been asked, did you go there? Of what use to civilization
can this lifeless continent be?... expeditions contributed something to the
accumulating knowledge of the Antarctic... that helps us thrust back further
the physical and spiritual shadows enfolding our terrestrial existence. Is it
not true that one of the strongest and most continuously sustained impulses
working in civilization is that which leads to discovery? As long as any part
of the world remains obscure, the curiosity of man must draw him there, as
the lodestone draws the mariner's needle, until he comprehends its secret”
Richard E. Bryd
Explorer
(1888-1957)
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List of publications
Phygoscelis papua
“There is a pleasure in the pathless woods, There is a rapture on the lonely
shore, There is society, where none intrudes, By the deep sea, and music in
its roar: I love not man the less, but Nature more, From these our interviews,
in which I steal From all I may be, or have been before, To mingle with the
Universe, and feel What I can ne'er express, yet cannot all conceal.”
George Gordon Byron
English poet and politician
(1788 – 1824)
List of publications
Peer-reviewed articles
1.
2.
3.
4.
5.
Pasotti, F., De Troch, M., Raes, M. and Vanreusel, A.: Feeding ecology
of shallow water meiofauna: insights from a stable isotope tracer
experiment in Potter Cove, King George Island, Antarctica, Polar Biol.,
35(11), 1629–1640, doi:10.1007/s00300-012-1203-6, 2012.
Pasotti, F., Convey, P. and Vanreusel, A.: Potter Cove, west Antarctic
Peninsula, shallow water meiofauna: a seasonal snapshot, Antarct.
Sci., 10, 1–10, doi:10.1017/S0954102014000169, 2014a.
Pasotti, F., Manini, E., Giovannelli, D., Wölfl, A.-C., Monien, D.,
Verleyen, E., Braeckman, U., Abele, D. and Vanreusel, A.: Antarctic
shallow water benthos in an area of recent rapid glacier retreat, Mar.
Ecol., doi:10.1111/maec.12179, 2014b.
Pasotti, F., Saravia, L.A., De Troch, M., Tarantelli, M.S., Sahade, R. and
Vanreusel A.: Benthic trophic interactions in an Antarctic shallow water
ecosystem affected by recent glacier retreat, Submitted to
Biogeosciences, submitted.
Pasotti F., De Troch, M. and Vanreusel, A.: “To cope or not to cope?”
Can Antarctic meiofauna cope with impacts from glacier-retreat?
Insights from two laboratory experiment, In preparation.
Poster presentations
1.
2.
3.
4.
5.
Raes, M., Pasotti, F., Vanreusel, A.: Antarctic meiofauna coping with
change, Workshop on the response of marine and terrestrial biota
along the Western Antarcic Peninsula to climate change and the
global context of the observed change, Mądralin (Warsaw), Poland,
2009.
Pasotti, F., Raes, M., De Troch, M. and Vanreusel, A.: Investigating the
responses of Potter Cove meiofauna from a climate change
perspective: an experimental approach, SCAR conference, Buenos
Aires, Argentina, 2010.
Pasotti, F. and Vanreusel A. : Investigating the responses of Potter
Cove meiofauna from a climate change perspective, APECS
symposium, Ghent, Belgium, 2012.
Pasotti, F.: Antarctique benthos et le recul des glaciers, Bringing the
Poles to Brussels, APECS, 2013.
Pasotti, F. and Vanreusel, A.: “To cope or not to cope” Potter Cove
(west Antarctic Peninsual) shallow water benthos under glacier retreat
241
List of publications
6.
forcing, Fifteenth International Meiofauna Conference (Fiftimco), Seoul,
South Korea, 2013.
Pasotti, F.: L’étude du benthos, Belgica Day, Brussels, Belgium, 2014.
Oral presentations
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
Pasotti, F. and Vanreusel A.: BIANZO II climate change effects on
benthos review paper: overview on Nematodes, BIANZO II Coping
with Change meeting, Ghent, Belgium, May 2009.
Pasotti, F., Raes, M., De Troch, M. and Vanreusel, A.: Investigating
the responses of Potter Cove meiofauna from a climate change
perspective: an experimental approach, Fourteenth International
Meiofauna Conference, Ghent, Belgium, 2009.
Pasotti, F. and Vanreusel A.: BIANZO II and Imcoast projects:
continuity in meiobenthic Antarctic research, BIANZO II Workshop,
Ghent, Belgium, September 2009.
Pasotti, F.: Jubany 2009/2010 : meiobenthos, Imcoast project
meeting, Bremerhaven, Germany, 2010.
Pasotti, F. and Vanreusel A.: How do extreme environments cope
with change: a focus on Antarctica, Instituut voor Permanente
Vorming, Onderzoek en Milieu, Ghent, Belgium, 2011.
Pasotti, F.: Antarctic and Arctic: extreme environments ina changing
world, Natural Sciences Museum, Brescia, May 2011.
Pasotti, F. and Vanreusel A.: Potter Cove meiofauna: ho they cope
with change? Imcoast workshop, Buenos Aires, Argentina, April
2012.
Pasotti, F.: Oceans and ecological footprint, Natural Sciences
Museum, Brescia, May 2012.
Pasotti, F., Vanreusel A. and Ingels, J.: Unraveling the benthic
response to climate change, Imcoast workshop, Bremerhaven,
Germany, November 2012.
Pasotti, F. and Vanreusel, A.: The Marbiol in the west Antarctic
Peninsula: the Imcoast project and our contribution for a better
understanding of Potter Cove (King George Island, Antarctica)
meiobenthos, Decembss Symposium, Ghent, Belgium, 2012.
Pasotti, F.: Oceans: What can We do? International Schools Lecture
to high school students, May 2013.
Pasotti F., De Troch, M. and Vanreusel, A.: “To cope or not to cope”?
Shallow water benthos under glacier retreat forcing, Fifteenth
International Meiofauna Conference, Seoul, South Korea, 2013.
242
List of publications
13.
14.
15.
Pasotti, F.: Oceans and Emptiness: human impact from science to
ethics, International Schools lecture to middle school students, May
2014.
Pasotti F. and Vanreusel, A.: Inbenthic fauna, a stable isotope
dataset, Imconet Food-Web modelling Workshop, Ghent, Belgium,
2014.
Pasotti F. and Vanreusel, A.: Benthic spatial and temporal dynamics
in relation to change, Imconet spatial modelling Workshop,
Bremerhaven, Germany, 2014.
Reports
1.
2.
3.
4.
5.
6.
Pasotti F. and Vanreusel A.: Report of scientific activity Jubany
2009/2010, pp 25, 2010.
Pasotti F.: IWT 1st year project progress report, pp 22, 2010.
Ingels, J., Pasotti F. and Vanreusel, A.: Imcoast final report, FWO projects,
pp 12, 2012.
Pasotti, F.: GleMeANT: effects of Glacial erosion on Meiobenthic
community of an ANTarctic bay, final report, IWT final report, pp 11,
2013.
Abele D., et al.: PolarCLIMATE project: Imcoast progress/final year report,
pp 104, 2013.
Pasotti F.: Bremerhaven Imconet spatial modeling workshop: an overview
of the progress, pp 9, 2014.
243